Lichens and Their Allies Past and Present

Honegger, Rosmarie

doi:10.1007/978-3-031-16503-0_6

Rosmarie Honegger⁷

Part of the book series: The Mycota ((MYCOTA,volume 5))

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Abstract

This chapter gives an overview on (1) lichen-forming fungi, lichen photobionts and peculiarities of lichen symbiosis such as gains and losses of lichenization, species concepts, specificity, morphodemes and morphotype pairs, non-lichen mutualistic fungal interactions with unicellular algae and cyanobacteria and mycophycobioses; (2) the mycobiont–photobiont interface, water relations and gas exchange, mycobiont-derived secondary metabolites and the accumulation of heavy metals or radionuclides; (3) the microbiome of lichen thalli, i.e. the bacteriome (epi- and endolichenic bacteria), lichenicolous and endolichenic fungi, lichenicolous lichens and the virome of lichens and their allies; (4) fossil lichens and their microbiome; (5) lichen–animal interactions such as the micro- and mesofauna of lichen thalli, lichenivory in invertebrates and vertebrates, endo-and epizoochory; (6) lichenomimesis in animals and flowering plants.

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Lichens

Microbial communities of lichens

Article 01 May 2017

Introduction

Keywords

1 Introduction

Lichens are the symbiotic phenotype of nutritionally specialized fungi, ecologically obligate biotrophs which acquire fixed carbon from a population of minute photobiont cells (Honegger 1991a, b). Lichen-forming fungi (also referred to as lichen mycobionts) are, like plant or animal pathogens or mycorrhizal fungi, a polyphyletic, taxonomically diverse group of nutritional specialists, but are otherwise normal representatives of their fungal classes. They differ from non-lichenized taxa by their manyfold adaptations to symbiosis with a population of minute photobiont cells (Honegger 2009). Lichenization is an ancient and very successful nutritional strategy, approximately 17% of extant fungal species being lichenized (Lücking et al. 2017a).

Lichens were the first mutualistic symbiosis discovered. The Swiss botanist Simon Schwendener (1829–1919) realized that the thallus of lichens is built up by a fungus which harbours a population of genetically different, minute green algal or cyanobacterial cells in its thalline interior (Schwendener 1867, 1869; Honegger 2000). Upon closer examination, lichen thalli represent not a dual or triple symbiosis of a C-heterotrophic partner, i.e., a lichen-forming fungus (the mycobiont) and a photoautotrophic partner, either a green alga and/or a cyanobacterium (the photobiont, also termed cholorobiont or cyanobiont, respectively), but consortia with an unknown number of participants (Fig. 6.1a–b; Honegger 1991a, b) or complex ecosystems, respectively (Hawksworth and Grube 2020). Lichenicolous and endolichenic fungi and bacterial epi- and endobionts are very common and widespread, their taxonomic affiliation and potential roles for the symbiosis having been intensely studied in the last decades (see Sects. 6.5.1–6.5.5). Endolichenic fungal and actinobacterial symbionts and epithalline bacteria were already present in Chlorolichenomycites devonicus, a fossil lichen of the Early Devonian (ca. 415 Ma old, see Sect. 6.6.2; Honegger et al. 2013a).

Two micrographs depict the sticta sylvatica. a. The labeled layers are the upper cortex, photobiont, medullary, and lower cortex. b. The labeled layer are bacteria, cyanobacterial, fungal hyphae, and testate amoeba. — **Fig. 6.1**

As pointed out by Hawksworth (2016), there is no need to change the concept of lichen in the light of these findings. The term symbiosis, as defined by de Bary (1879), refers to genetically different organisms living together, neither the outcome of their interaction (parasitic, commensalistic or mutualistic relationships, the term mutualism having been introduced by Van Beneden in 1875) nor the number of organisms involved was defined.

Until the end of the twentieth century, the taxonomy of lichen-forming fungi and their photobionts was based on morphological, chemical and structural characters. In the twenty-first century, molecular tools, bioinformatics and rapidly growing databases facilitated the study of the inter- and intraspecific diversity of lichen-forming fungi and their photobionts, their phylogenies, but also the intrathalline biodiversity and the pro- and eukaryotic microbiome of lichen thalli.

2 Lichen-Forming Fungi (LFF)

2.1 Gains and Losses of Lichenization

Lichenization was repeatedly acquired (14–23 lichenization events in the Ascomycota, 6–7 in the Basidiomycota), but also repeatedly lost in favour of a saprotrophic, lichenicolous or parasitic mode of nutrition (Lücking et al. 2017a, b; Nelsen et al. 2020). Examples of relatively recently de-lichenized taxa among the Lecanoromycetes are the lichenicolous Raesaenenia huuskonenii (syn. Protousnea huuskonenii, Parmeliaceae, Lecanorales; Divakar et al. 2015; Fig. 6.6h–i) or the lignicolous Xylographa constricta (Baeomycetaceae, Baeomycetales; Spribille et al. 2014).

2.2 Species Concepts and Phylogenies

The genus and species name of a lichen refers to the fungal partner, irrespective of it being symbiotic in nature or axenically cultured apart from its photobiont (Hawksworth 2015). Attempts to refer to the aposymbiotically cultured mycobiont as …-myces (e.g. Xanthoriomyces parietinae for aposymbiotically cultured Xanthoria parietina; Thomas 1939) are obsolete. The photoautotrophic partner(s) of lichens have their own names and phylogenies. Traditionally, lichens were described on the basis of morphological (morphospecies) and chemical characters (secondary metabolites: chemospecies). Molecular tools provided novel insights into phylogenies, evolutionary trends and taxonomic relationships in general and in questions related to the delimitation of species in particular (Lücking et al. 2021). Many well-known morphospecies turned out to comprise either cryptic species or morphodemes (see Sects. 6.2.3 and 6.2.4).

In their 2016 classification, Lücking and colleagues listed 19,387 accepted species of lichenized fungi in 995 genera, 115 families, 39 orders and eight classes, the vast majority being ascomycetes; Lecanoromycetes, the largest and most anciently lichenized class among extant ascomycetes, comprises more than 15,100 spp. (Lücking et al. 2017a, b). Only 172 species, 15 genera, five families, five orders in one class belong to the basidiomycetes (Lücking et al. 2017a, b), but molecular data of more than 300 species of basidiolichens were not yet published. In the meantime, new taxa of basidiolichens have been described (Coca et al. 2018; Dal-Forno et al. 2019; Lücking et al. 2022). However, large numbers of species and genera of lichenized asco- and basidiomycetes await molecular analysis.

Based on molecular datasets, large numbers of new species, numerous new genera, families, few orders (e.g., the ascolichen orders Eremithallales; Lücking et al. 2008, Leprocaulales; Lendemer and Hodkinson 2013, Collemopsidales; Pérez-Ortega et al. 2016, or the basidiolichen order Leptostromatales; Hodkinson et al. 2014) and classes (e.g. Lichinomycetes; Reeb et al. 2004; Coniocybomycetes; Prieto et al. 2013) have been described. Within 6 years (2010–16), more than half of all genera of LFF were subjected to changes (Lücking et al. 2017a, b), and this work continues. Intense biodiversity analyses have been performed in areas and ecosystems which have so far been poorly investigated. An example is the TICOLICHEN project in Costa Rica, the major tropical lichen biodiversity inventory initiated in 2002 by Robert Lücking and colleagues (Lücking et al. 2004).

Molecular phylogenies give fascinating insights into evolutionary processes and biogeographic developments. Examples are (1) the calicioid ascomycetes, predominantly crustose species with prototunicate asci whose ascospores achieve maturation in a mazaedium. Their asci disintegrate before the ascospore wall is fully differentiated, spore maturation being completed in a powdery mass, the mazaedium, at the surface of the ascoma (Honegger 1985). Based on this feature, mazaediate ascomycetes were formerly classified in the order Caliciales within the Lecanoromycetes. Today, mazaediate taxa fall into four classes: Lecanoromycetes, Eurotiomycetes, Arthoniomycetes and Coniocybomycetes (Prieto et al. 2013; Wijayawardene et al. 2020). (2) the leprose lichens with no sexual reproductive stages and morphologically very simple thalli built up by loosely interwoven hyphae which secrete interesting secondary metabolites and are in contact with green algal cells, forming a powdery mass with no stratification. Today leprose lichens of the genus Lepraria are classified in the Stereocaulaceae, Leprocaulon in the Leprocaulaceae (Lecanoromycetes; Lendemer and Hodkinson 2013), Botryolepraria in the Verrucariaceae (Eurotiomycetes; Kukwa and Pérez-Ortega 2010) and Andreiomyces in Andreiomycetaceae (Arthoniomycetes; Hodkinson and Lendemer 2013). Moreover, leprose thalli are formed in fertile taxa such as Chrysothrix (rarely fertile; Chrysothrichaceae, Arthoniomycetes; Nelsen et al. 2009; Liu et al. 2018) or in Chaenotheca furfuracea (syn. Coniocybe f.; Coniocybaceae, Coniocybomycetes). (3) Phylogeographic studies provided insights into large-scale population histories, e.g., of Lobaria pulmonaria in North America or in the post-glacial re-colonization of the Alps (Lerch et al. 2018; Allen et al. 2021), or of the cosmopolitan Psora decipiens (Leavitt et al. 2018).

2.3 Species Pairs and Cryptic Species

The species pair concept in lichenology is based on the observation that some morphologically similar lichens differ in their reproductive mode, i.e., are either fertile or asexually reproducing, the fertile stage having been assumed to be the primary species (Crespo and Pérez-Ortega 2009). Many sexual–asexual species pairs turned out to represent a monophyletic lineage. The Porpidia flavocoerulescens and P. melinodes species pair was hypothesized to maintain asexual reproduction under optimal conditions, but sexual reproduction and re-lichenization for escaping from a suboptimal symbiosis (Buschbom and Mueller 2006). In the presumed Letharia columbiana (fertile) and L. vulpina species pair L. columbiana turned out to comprise five cryptic taxa, hybridization and polyploidization included (Kroken and Taylor 2001; Altermann et al. 2016; Ament-Velásquez et al. 2021).

Many other morphospecies turned out to comprise numerous cryptic species (e.g. Pseudocyphellaria crocata comprising 13 spp.; Lücking et al. 2017a, b), the most extreme examples being (1) the lichenized basidiomycete Dictyonema glabratum (syn. Cora pavonia), which comprises at least 126 taxa (Lücking et al. 2014, 2016; Moncada et al. 2019); upon closer examination these hidden basidiolichen species turned out to be morphologically distinct, although the differences are recognizable to the expert’s eye only. (2) the species complex of the cosmopolitan crustose lichenized ascomycete Lecanora polytropa comprises up to 103 cryptic species (Zhang et al. 2022).

2.4 Morphodemes and Morphotype Pairs (= Photosymbiodemes)

Morphodemes are formed by phylogenetically distinct taxa which differentiate the same morphotype; examples are found in the Sticta filix (Ranft et al. 2018) or the Sticta weigelii complexes (Moncada et al. 2021). On the other hand, morphologically distinct lichens, some of which had been classified in different genera, turned out to be congeneric or even conspecific. This phenomenon was first observed in tripartite lichens with a morphologically distinct cyanobacterial and a green algal morphotype, i.e., in Ricasolia amplissima (lobate chloromorph with cephalodia) and Dendriscocaulon bolacinum (fruticose cyanomorph; Dughi 1937), chimaeric forms included (James and Henssen 1976). Photosymbiodemes formed by lobate chloromorphs and fruticose, dendriscocauloid cyanomorphs occur in various peltigeralean genera (Sticta, Lobaria, Ricasolia; Paulsrud et al. 1998; Magain et al. 2012; Tønsberg et al. 2016; Ranft et al. 2018). Photosymbiodemes with morphologically similar lobate chloro- and cyanomorphs occur in Peltigera spp. (Goffinet and Bayer 1997; see Fig. 15.1f in Honegger 2012).

Vastly different morphologies formed by the same fungal species were found in Endocena and Chirleja spp. (Icmadophilaceae); their coccoid green algal photobiont was not investigated (Fryday et al. 2017). A very peculiar morphotype pair is formed by two crustose lichens with either a trebouxioid or a trentepohlioid green algal photobiont (Ertz et al. 2018). The sterile, sorediate Buellia violaceofusca (formerly classified in Lecanoromycetes), which associates with different phylospecies of the genus Trebouxia (Trebouxiophyceae), and the fertile Lecanographa amylacea (Arthoniomycetes) with a Trentepohlia photobiont (Ulvophyceae) turned out to be conspecific. This was the first example of a lichen-forming ascomycete with a trebouxioid and a trentepohlioid morphotype. As in non-lichenized fungi the species name refers to the sexually reproducing stage (teleomorph). Lecanographa amylacea most likely captures trebouxioid photobiont cells from adjacent crustose or leprose lichens to form the sorediate (anamorphic) morphotype (Ertz et al. 2018).

2.5 Non-lichen Mutualistic Fungal Interactions with Cyanobacteria and Unicellular Green Algae

It is astonishing that no Zygomycetes, Glomeromycetes or Chytridiomycetes are among the extant LFF. However, in each of these classes, which are phylogenetically older than asco- and basidiomycetes, at least one example of a mutualistic symbiosis with either a cynobacterial or green algal partner was reported.

The Glomeromycetes Geosiphon pyriformis forms a very ancient endocyanosis with Nostoc sp. at the soil surface, the cyanobacterial photobiont being incorporated in hyphae which subsequently differentiate a bladder at the soil surface. The Nostoc filaments are kept in membrane-bound vesicles (perialgal vacuoles) in the fungal cytoplasm where they undergo cell division, are photosynthetically active and fix atmospheric N₂. The first glomeromycetan monosaccharide transporter characterized was shown to function at the symbiotic interface of Geosiphon with its cyanobacterial partner (Schüssler et al. 2006, 2007; review: Schüssler 2012).

Under certain environmental conditions, mutualistic interactions between non-lichenized fungi and algae are formed without prior co-evolutionary adaptation. The zygomycete Mortierella elongata and the unicellular green alga Nannochloropsis oceanica are both biotechnologically cultured on large scale to produce lipids for biofuel. In co-culture, both partners interact, the algal cells adhere to the fungal hyphae and finally become internalized, leading to a green mycelium (Du et al. 2019). This situation resembles the Geosiphon–Nostoc symbiosis, although a green alga instead of a cyanobacterium is involved.

Chytrids are saprobes or parasites of fungi, algae, plants and amphibians (reviews: Powell 2017; Longcore et al. 2020). Parasites of phytoplankton attack free-living algal species (Van den Wyngaert et al. 2018) and have a devastating effect on commercially grown algal cultures (Hoffman et al. 2008; Longcore et al. 2020). The chytrid Rhizidium phycophilum forms a facultative mutualism with a Bracteacoccus sp. (Sphaeropleales; syn. Chlorococcales) and can only be cultured in the presence of this zoosporic green algal species. The alga is not parasitized, it even grows larger and more prolific and reveals an up to eight-fold increase in biovolume in co-culture as compared to axenic culture under the same conditions. This is the first report of a mutualistic interaction between a chytrid and a green alga (Picard et al. 2013).

The ascomycetous yeast Saccharomyces cerevisiae (Saccharomycotina) and filamentous ascomycetes such as Aspergillus nidulans (Eurotiomycetes) form mutualistic interactions with the flagellate unicellular Chlamydomonas reinhardtii (Chlamydomonadales, Chlorophyceae), although with different levels of productivity and without differentiating thallus-like structures as seen in lichen-forming ascomycetes (Hom and Murray 2014) However, C. reinhardtii cells are protected by A. nidulans from bacteria and their toxins (Krespach et al. 2020). Two extremely halotolerant organisms, the black yeast Hortaea werneckii (Teratosphaeriaceae, Capnodiales), which can switch from filamentous growth to the yeast form, and the flagellate unicellular green alga Dunaliella atacamensis (Chlamydomonadales), were found to interact in co-cultures (Muggia et al. 2020b). Despite close fungal–algal contacts, neither a mutual benefit, nor an antagonistic interaction was observed. Nevertheless, such heterotroph–autotroph contacts might be the beginning of a stable symbiotic interaction.

2.6 Mycophycobioses

Mycophycobioses are mutualistic fungal interactions with quantitatively predominant, multicellular algal hosts. Mycophycias ascophylli (Capnodiales incertae sedis, Dothideomycetes; Toxopeus et al. 2011; Wijayawardene et al. 2020) inhabits the intertidal brown algae Pelvetia canaliculata and Ascophyllum nodosum (Fucales, Phaeophyceae) in the upper littoral of the Atlantic, only its minute ascomata being visible at the surface of the seaweed’s receptaculum (gamete-producing structure; Fig. 6.2), their very thin vegetative hyphae being best visible in ultrathin sections (Xu et al. 2008). In fresh water, Phaeospora lemaneae (syn. Leptosphaeria lemaneae; Verrucariales, Eurotiomycetes) associates with the red alga Lemanea fluviatilis (Batrachospermales, Rhodophyta; Brierley 1913; Hawksworth 2000). M. ascophylli improves the desiccation tolerance of the zygotes of its brown algal host A. nodosum (Garbary and London 1995). Improved desiccation tolerance was also hypothesized for the red algal host L. fluviatilis upon infection with P. lemaneae (Hill 1992), but experimental data are missing.

Three images a. Gametes are produced in conceptacles in receptacles. b. Gametes ooze out of the ostiole, point to ascomata, and recognize dots and c. Stained semi-thin section with ascoma. — **Fig. 6.2**

About 100 species of fungal endophytes of seaweeds (Phaeophyta, Rhodophyta, Chlorophyta) were identified, some of them producing bioactive secondary metabolites (Noorjahan et al. 2021).

2.7 Secondary Metabolites

Lichen thalli are a rich source of interesting polyphenolic secondary metabolites, many of them with bioactive properties. Most of them are produced by the mycobiont, others by endolichenic fungi or by epi- or endolichenic bacteria (see below). Lichen compounds evolved early in the radiation of filamentous fungi (Armaleo et al. 2011). Polyketide synthase (PKS) genes were most likely gained by horizontal gene transfer from actinobacteria before the radiation in Leotiomyceta, which gave rise to the extant crown group of Ascomycota (Schmitt and Lumbsch 2009). PKS genes have been repeatedly lost in non-lichenized ascomycetes but retained and even duplicated in most lichenized ascomycetes (Schmitt and Lumbsch 2009). However, also in lichenized taxa were PKS gene clusters repeatedly lost (Pizarro et al. 2020).

The chemistry of mycobiont-derived secondary metabolites, the so-called lichen products, has attracted considerable interest, with a large body of literature having been published from the late nineteenth century onwards (e.g. Zopf 1896, 1907; Asahina and Shibata 1954; Culberson 1969, 1970; Culberson and Elix 1989; Culberson et al. 1977; Huneck and Yoshimura 1996; Huneck 2001; Elix and Stocker-Wörgötter 2008); a database of high-resolution tandem mass spectrometry (MS/MS) spectra for lichen metabolites is available (Olivier-Jimenez et al. 2019).

It is not known in which form the secondary metabolites are excreted by the fungal cells (possibly as glycosides?). In their soluble form, they are passively translocated into the apoplastic continuum during the wetting and drying cycles and crystallize either at on the surface of ascomata (e.g. bellidiflorin in Cladonia spp.; Fig. 6.3a, or haemoventosin in Ophioparma ventosa; Fig. 6.3b–c), on the thallus surface (e.g. anthraquinones such as parietinic or solorinic acid, pulvinic acid derivatives such as vulpinic or rhizocarpic acid, or depsides such as atranorin), many of them giving the thallus its characteristic colouration; others (e.g. depsidones such as physodic or protocetraric acid) crystallize on the surface of medullary hyphae and even on green algal photobiont cells in the thalline interior (Fig. 6.3d; Honegger 1986b). In soredia, mycobiont and photobiont cells are often heavily loaded with crystalline secondary metabolites which enhance their hydrophobicity (Fig. 6.3e). Crystalline lichen products are almost insoluble in aqueous systems below pH 7. Many mycobiont-derived secondary metabolites are produced in sterile, aposymbiotic culture (Thomas 1939; Yamamoto et al. 1985; Honegger and Kutasi 1990; Culberson and Armaleo 1992; Stocker-Wörgötter et al. 2013; Díaz et al. 2020; Jeong et al. 2021, etc.).

Five images depict the biosynthesis of metabolites. a. Usnic and squamatic acid in ascomata. b. and c. The haemoventosin in the ascomata. c. The acid is usnic, thamnolic, miriquidic, and divaricate. d. Algal layer in cryofixed. e. Hyphae and algal cells of soredia. — **Fig. 6.3**

Numerous PKS gene clusters have been characterized (e.g. Miao 1999; Armaleo et al. 2011; Wang et al. 2014; Bertrand and Sorensen 2018; Bertrand et al. 2018; Calchera et al. 2019; Pizarro et al. 2020; Sveshnikova and Piercey-Normore 2021; Gerasimova et al. 2022; Singh et al. 2022), many of them being not expressed in the lichen thallus. Thus, LFF have an unexplored biosynthetic potential (Bertrand et al. 2018; Gerasimova et al. 2022).

As most LFF are slow-growing organisms, lichen-derived PKS genes were transferred into fast-growing non-lichenized ascomycetes. A Pseudevernia furfuracea-derived PKS gene was successfully expressed in baker’s yeast (S. cerevisiae), the depside lecanoric acid being synthesized (Kealey et al. 2021). The transfer of lichen-derived PKS genes in filamentous ascomycetes such as Aspergillus spp. lead to successful transcription (Wang et al. 2016), but for unknown reasons, secondary products were often not synthesized (Gagunashvili et al. 2009; Yang et al. 2018; Bertrand and Sorensen 2019a, b).

Lichens have been used in traditional medicine around the globe (Crawford 2019). In the last decades, a large body of literature was published on interesting pharmaceutical properties of β-glucans such as lichenans (e.g. Caseiro et al. 2022), important cell wall components of Lecanoromycetes (Honegger and Haisch 2001), and of a wide range of lichen-derived secondary metabolites with antibiotic, anti-inflammatory, antiproliferative, antiviral, antineurodegenerative, antioxidant activities, etc. (various authors in Ranković 2019; reviews: Boustie and Grube 2005; Boustie et al. 2011; Bhattacharyya et al. 2016; Studzinska-Sroka et al. 2017; Ingelfinger et al. 2020; Ureña-Vacas et al. 2021). Best investigated is usnic acid (Macedo et al. 2021; Xu et al. 2022), whose antibacterial properties were detected by Stoll et al. (1947).

3 Lichen Photobionts

3.1 Diversity and Specificity

In her 1988 compilation, Tschermak-Woess listed 44 genera of lichen photobionts: 15 cyanobacterial, 27 chlorophycean, one xanthophycean and one phaeophycean (Tschermak-Woess 1988). All of these taxa had been described on the basis of morphological characters. From 1989 onwards, molecular tools, applied either to cultured (aposymbiotic) photobiont isolates or to whole thallus DNA preparations, revolutionized our knowledge of lichen photobiont diversity. In 2021, Sanders and Masumoto summarized the current state of the art. They listed 52 genera of lichen photobionts: 13 cyanobacterial, 36 chlorophycean, two xanthophycean and one phaeophycean (Sanders and Masumoto 2021). New photobiont genera had been described (e.g. Heveochlorella, Trebouxiophyceae; Sanders et al. 2016, or Bracteacoccus, Chlorophyceae; Masumoto 2020).

The Verrucariales (three families, 55 genera, >800 spp.), which comprises terrestrial, but also numerous fresh water and marine species, harbours the highest photobiont diversity. The only phaeophycean (Petroderma maculiforme in Wahlenbergiella tavaresiae) and xanthophycean photobionts (Heterococcus sp. in Verrucaria and Hydropunctaria spp., Xanthonema sp. in Staurothele clopimoides) are symbiotic with verrucarialean taxa (review: Sanders and Masumoto 2021). Many photobiont taxa associate exclusively with marine LFF. Examples are the cyanobacterial Hyella sp. in Collemopsidium halodytes (syn. Arthopyrenia h., Xanthopyreniaceae) or Rivularia sp. in Lichina pygmaea and L. confinis (Lichinales, Lichinomycetes; see Figs. 15.1.p-r in Honegger 2012). Among marine green algal photobionts of marine Verrucariaceae are the ulvophycean Blidingia minima (with Turgidosculum ulvae; Pérez-Ortega et al. 2018), Halophilum ramosum, Lithotrichon pulchrum, Paulbroadya petersii, Pseudendoclonium submarinum and Undulifilum symbioticum (with Hydropunctaria and Wahlenbergiella spp.), or the trebouxiophycean Prasiola spp. in Mastodia tessellata (Sanders and Masumoto 2021; Černajová et al. 2022).

The genus Trebouxia harbours the most common and widespread unicellular green algal photobionts of LFF; Trebouxia spp. are photobionts of Parmeliaceae (>2760 spp.; Lücking et al. 2017a, b), Teloschistaceae (>810 spp.), etc. Tschermak-Woess (1988) listed seven species, Sanders and Masumoto (2021) 27 plus several unnamed phylospecies and clades, whence five had been transferred from Pseudotrebouxia (which no longer exists), and 19 species have been newly described from 1989 onwards. In Asterochloris, the second-most common genus, Tschermak-Woess (1988) listed one species, Sanders and Masumoto (2021) 18 plus several unnamed phylospecies and clades; four of these Asterochloris spp. had been transferred from Trebouxia to Asterochloris (A. erici, A. glomerata, A. italiana, A. magna). Asterochloris spp. are photobionts of Cladonia and Stereocaulon spp. and many other taxa (Sanders and Masumoto 2021), new phylogenetic lineages having been recently described (Kosecka et al. 2021).

Trebouxia and Asterochloris spp. are characterized by their large, lobate chloroplast with central pyrenoid. Chloroplast lobation and its interspecific variation was visualized with Confocal Laser Scanning Microscopy (CLSM; Trebouxia: Muggia et al. 2012; Bordenave et al. 2021; Asterochloris: Škaloud and Peksa 2008; Moya et al. 2015; Škaloud et al. 2015; Kim et al. 2017).

As in LFF, considerable cryptic diversity was found among lichen photobionts; examples in Trebouxia (Singh et al. 2019; Muggia et al. 2020a, b; Kosecka et al. 2022), Coccomyxa (Darienko et al. 2015; Malavasi et al. 2016), Dictyochloropsis or Symbiochloris, respectively (Dal Grande et al. 2014; Škaloud et al. 2016), Trebouxiophyceae (Metz et al. 2019) or Trentepohliales (Borgato et al. 2022).

Unfortunately lichen thalli cannot be routinely resynthesized by combining cultured myco- and photobionts. Therefore, the specificity and selectivity of the symbiosis cannot yet be investigated under controlled experimental conditions. Our knowledge about the range of acceptable partners per fungal species or genotype is based on analyses of specimens collected in nature. Ideally, sampling was done over the whole geographic range of the fungal species.

Many (the majority?) of LFF with trebouxioid or trentepohlioid photobionts associate with more than one algal species or genotype; examples are Xanthoria parietina with Trebouxia decolorans or T. arboricola (Nyati et al. 2014) or cosmopolitan species of Stereocaulon, Cladonia or Lepraria, which reveal low specificity towards their photobiont (Kosecka et al. 2021). In Cladonia spp., external factors such as climate or soil chemical properties have an impact on photobiont selection (Pino-Bodas and Stenroos 2021; Škvorová et al. 2022); severe heavy metal pollution even induced a switch from Asterochloris to Trebouxia spp. (Osyczka et al. 2020).

Based on light microscopy studies, the algal cell population of lichen thalli was assumed to be uniform, but molecular tools revealed intrathalline photobiont diversity. Different photobiont species or genotypes of the same photobiont may grow within the same thallus (for special relationships such as morphotype pairs, see Sect. 6.2.4, or tripartite lichens, see Sect. 6.3.2, respectively). In all thalli of Ramalina farinacea were two unnamed Trebouxia spp. found with different physiological properties (Casano et al. 2011; del Hoyo et al. 2011). In 45% of Evernia mesomorpha were multiple genotypes of one Trebouxia species found (Piercey-Normore 2006). In 30 out of 104 thalli of Tephromela atra or Rhizoplaca melanophthalma, respectively, were co-occurring Trebouxia spp. found (de Carolis et al. 2022). Only once were two genotypes of T. decolorans found in a thallus of X. parietina (Nyati et al. 2014).

Some Trebouxia photobionts were found free-living in nature (Bubrick et al. 1984), but they are not common members of aerophilic algal communities. In contrast, photobionts of the genera Apatococcus, Stichococcus, Coccomyxa, Elliptochloris, Myrmecia, Symbiochloris, Prasiola (all Trebouxiophyceae) or Trentepohlia (Ulvophyceae) are common in the free-living state, many of them having been found in soil samples along an altitudinal gradient (Stewart et al. 2021) or in biological soil crust communities (Flechtner et al. 2013; Borchhardt et al. 2017). This should be kept in mind when exploring microalgal diversity in whole thallus extracts: adhering fragments of symbiotic propagules from other lichens or free-living algae might be included. Ideally, lichen photobionts are isolated from the algal layer of dissected thallus fragments and cultured under sterile conditions prior to genetic analysis (Nyati et al. 2013, 2014).

3.2 Tripartite Lichens

(a)
Lichens with a mixed photobiont layer comprising green algae and cyanobacteria. In a few lichens, the photobiont layer comprises a green algal and a cyanobacterial partner, both being photosynthetically active. Examples are (a) Euopsis granatina with Trebouxia aggregata as a green algal and Gloeocapsa sanguinea as cyanobacterial photobiont (Büdel and Henssen 1988); (b) Muhria urceolata (Jørgensen and Jahns 1987, syn. Stereocaulon urceolatum; Högnabba 2006) and (c) various cyanomorphs of Pseudocyphellaria spp. (Ps. rufovirescens, Ps. lividofusca, Ps. dissimilis, Ps. hookeri, Ps. crocata) and Sticta fuliginosa, all with Nostoc sp. (Henskens et al. 2012). In some of these peltigeralean species the green algal partner was detected when ribitol, the characteristic carbohydrate produced by numerous green algal photobionts (Hill 1976; Honegger 1997), was identified among the photobiont-derived mobile carbohydrates in the thalli (Henskens et al. 2012).
(b)
Cephalodiate species are green algal lichens which capture repeatedly a diazotrophic cyanobacterium as a secondary photobiont (see Fig. 15.16 a–k in Honegger 2012), either at the upper (e.g. in green algal Peltigera spp.) or at the lower surface (e.g. in Solorina spp.) or at both surfaces (Lobaria pulmonaria; Cornejo and Scheidegger 2013) and incorporate it in either an external (e.g. Peltigera aphthosa, Stereocaulon ramulosum) or internal cephalodium (e.g. Solorina crocea, Nephroma arcticum). Capture of a cyanobacterial partner occurs in young lobes of the green algal lichen, mature cephalodia being found in fully grown areas of the lobes (Cornejo and Scheidegger 2013). The cyanobacterial photobionts in cephalodia are photosynthetically active, i.e., satisfy their demands of fixed carbon, but are diazotrophic, i.e., reduce atmospheric N₂ into bioavailable ammonium, highest N₂ fixation rates being achieved under microaerobic conditions. In mature cephalodia of Peltigerales with Nostoc as the secondary photobiont, the percentage of heterocysts, i.e., the site of N₂ fixation, is elevated (up to 55%) as compared to either cyanobacteria as primary photobiont of cyanolichens (approx. 5–8%) or free-living Nostoc spp. (Englund 1977; Hyvärinen et al. 2002). It is particularly interesting to see how lichen mycobionts generate microaerobic conditions, optimal for N₂ fixation, by forming a dense cortex around external cephalodia, which differs anatomically from the thalline cortex (see Fig. 15.16d–f and i–k in Honegger 2012). By 3D imaging using X-ray computed tomography at the microscopy level (Micro-CT, allowing for non-destructive analysis of the 3D-geometry in solid specimens; Elliott and Dover 1982; Hunter and Dewanckele 2021), the cephalodia were quantified (Gerasimova et al. 2021); in Lobaria pulmonaria the internal cephalodia amounted for 0.73%, in Peltigera leucophlebia (external cephalodia) for 0.97% of thallus volume.
(c)
Cephalodiate species are found in all green algal Peltigerales (Peltigera and Solorina spp. etc. [Peltigeraceae] and Lobaria, Sticta, Pseudocyphellaria spp., etc. [Lobariaceae]), in all representatives of the genera Stereocaulon (Stereocaulaceae, Lecanorales), Placopsis (Trapeliaceae, Baeomycetales; Ott et al. 1997), but also in some crustose taxa such as Calvitimela aglaea (syn. Lecidea shushanii or Tephromela aglaea, respectively, Tephromelataceae, Lecanorales; Hertel and Rambold 1988; Bendiksby et al. 2015).

3.3 Cyanotrophy

Cyanotrophy, i.e., the close contact of lichens with free-living cyanobacterial colonies, first observed in Bryonora spp. (Poelt and Mayrhofer 1988), might be common and widespread among saxicolous, epiphytic and soil crust lichens (Elbert et al. 2012; Cornejo and Scheidegger 2016; Gasulla et al. 2020). The contacting lichen benefits from fixed nitrogen, as produced by diazotrophic cyanobacteria, as is also the case in bryophyte interactions with free-living cyanobacteria (Gavazov et al. 2010; Warshan et al. 2017). Epiphytic bryophyte–cyanobacteria associations can serve as a reservoir for lichen cyanobionts (Cornejo and Scheidegger 2016).

4 Peculiarities of Lichen Symbiosis

4.1 A. Symbiotic vs. Free-Living LFF

In nature, the majority of LFF are symbiotic, but physiologically they do not depend on lichenization. Soon after the discovery of lichen symbiosis by Schwendener (1867, 1869), the first culturing and resynthesis experiments with LFF and their photobionts were carried out (Stahl 1877; Bonnier 1886, 1889). From large numbers of lichen-forming ascomycetes, sterile cultures have been established, starting with either ascospores, soredia or hyphal fragments which had been scratched out of dissected thalli (e.g. Lange de la Camp 1933; Thomas 1939; Ahmadjian 1959, 1962; Honegger and Bartnicki-Garcia 1991; Crittenden et al. 1995; Stocker-Wörgötter 1995, etc.). Single-spore isolates derived from one meiosis (i.e. the content of one ascus) facilitated the analysis of mating type systems (Honegger et al. 2004a; Honegger and Zippler 2007; Scherrer et al. 2005). Thus, LFF are ecologically obligate, but physiologically facultative biotrophs. However, some LFF most likely acquire additional carbohydrates as saprotrophs. Hyphae of Icmadophila ericetorum or Baeomyces rufus on decaying wood grow deep into the substratum and penetrate the lignified cell walls (see Figs. 12 and 14 in Honegger and Brunner 1981). In large numbers of Lecanoromycetes, a whole arsenal of genes encoding enzymes for carbohydrate degradation was identified (Resl et al. 2022).

LFF are seldom macroscopically visible in a non-lichenized state in nature. Examples are (1) juvenile developmental stages of Rhizocarpon spp. (Rhizocarpales), recognizable as a strongly melanized, black prothallus in search of a compatible photobiont, or (2) the optionally lichenized Schizoxylon albescens (Ostropales) on the bark of Populus tremula, which grows as a saprobe on dead wood of poplar (Muggia et al. 2011), or (3) the lichenized Conotrema spp. and their non-lichenized, saprotrophic stage which had been described as Stictis spp., optional lichenization presumably allowing to increase the ecological amplitude (Wedin et al. 2004, 2005).

4.2 Morphogenetic Capacity of the Mycobiont

In order to keep their photoautotrophic partner photosynthetically active, LFF have to grow at the surface of the substrate, thus exposing their thallus to temperature extremes, illumination, ultra-violet (UV) radiation included and to continuous fluctuations in water content, i.e. to regular drying and wetting cycles. Many mycobiont-derived cortical secondary metabolites such as parietin or atranorin are autofluorescent, i.e. absorb UV light and transform it into longer wavelengths (Fernandez-Marin et al. 2018); therefore, they were assumed to protect the myco- and photobiont from UV damage and to provide the photobiont cell population with wavelengths matching the absorption spectra of photosynthesis; however, the latter hypothesis was not supported by experimental approaches (Fernandez-Marin et al. 2018). The biosynthesis of secondary metabolites is enhanced by seasonally or experimentally elevated UV radiation (BeGora and Fahselt 2001; Bjerke et al. 2002, 2005; Solhaug et al. 2009). However, there are yet unknown genetic factors causing quantitative differences in cortical secondary metabolites among thalli of the same species growing side by side (Bjerke et al. 2005; Itten and Honegger 2010).

Foliose, band-shaped or fruticose lichen thalli with internal stratification are the most complex vegetative structures in the fungal kingdom. However, less than half of all lichens reveal this morphology and anatomy, the majority forming either microfilamentous, microglobose, crustose, leprose, gelatinous or squamulose thalli with no internal stratification (see Figs. 15.1a–y and 15.8 a–e in Honegger 2012). Many crustose taxa grow within the uppermost zone of the substratum where they meet their photobiont; examples are Arthopyrenia halodytes (syn. Pyrenocollema h.) with cyanobacterial photobiont (Hyella spp.) in the calcareous shell of limpets (Patella spp., Mollusca) or barnacles (Cirripedia, Crustacea), Graphis spp. with trentepohlioid photobiont in bark, etc. (see Fig. 15.1a–b in Honegger 2012).

4.3 The Mycobiont–Photobiont-Interface

In all lichenized asco- and basidiomycetes, the photoautotrophic partner is located outside the contacting fungal hyphae, with different types of mycobiont–photobiont interfaces being differentiated, ranging from simple wall-to-wall apposition to transparietal (formerly termed intracellular) or intraparietal haustoria (Honegger 1986a, b, 1991a; see micrographs in Fig. 15.13 a–l in Honegger 2012). When compared with biotrophic plant pathogenic fungi such as rusts or powdery mildews or with arbuscular mycorrhizal fungi, which form lobate or arbuscular transparietal haustoria, i.e., a large exchange surface in close contact with the plasma membrane of the host cell, the mycobiont–photobiont contact site in lichen is surprisingly simple (see Fig. 1a–f in Honegger 1993): in intraparietal haustoria, as formed by Parmeliaceae, Teloschistaceae, Cladoniaceae, etc., the mycobiont does not pierce the cellulosic cell wall of the chlorobiont (Trebouxia or Asterochloris spp., respectively; see Fig. 15.13 a–l in Honegger 2012). A whole range of genes encoding carbohydrate-active enzymes and sugar transporters were identified in 46 representatives of Lecanoromycetes; these LFF would be able to enzymatically degrade the cellulosic cell wall of their photobiont; many of them are likely acquiring additional carbohydrates as saprotrophs (Resl et al. 2022).

Simple wall-to-wall apposition is found in asco- and basidiolichens with Coccomyxa or Elliptochloris chlorobionts; these incorporate enzymatically non-degradable, sporopollenin-like algaenans in a thin outermost cell wall layer (Honegger and Brunner 1981; Brunner and Honegger 1985; see Fig. 15.3 a–c in Honegger 2012).

4.4 Water Relations and Gas Exchange

LFF and their photobionts are poikilohydrous organisms (Greek poikilos: variable; Greek hydror: water) and as such unable to control their water relations. They survive fluctuations in water content between saturation and desiccation (less than 10% water dw⁻¹) unharmed and are metabolically dormant during drought stress events, but recover within few minutes upon rehydration (Scheidegger et al. 1995). During desiccation, the cyanobacterial and green algal cells shrivel and the fungal hyphae cavitate, as seen in Low Temperature Scanning Electron Microscopy preparations of frozen-hydrated specimens, but irrespective of these dramatic changes, the cellular membrane systems remain intact, as visualized in ultrathin sections prepared from cryofixed, freeze-substituted specimens in Transmission Electron Microscopy (Honegger and Peter 1994; Honegger et al. 1996; Honegger and Hugelshofer 2000; see Fig. 16.5a–c in Honegger 2009). Poikilohydrous water relations are also characteristic of lichenicolous and endolichenic fungi and lichen-associated bacteria.

In lichen thalli water and dissolved nutrients are passively taken up at the thallus surface by the conglutinate cortex and/or rhizinae with hydrophilic wall surfaces and passively translocated into the photobiont and medullary layers. As shown with LTSEM techniques, a flux of solutes occurs within the fungal apoplast, mostly in the thick, glucan-rich outer wall layer and underneath the thin hydrophobic wall surface layer (Honegger and Peter 1994); the latter is built up primarily by mycobiont-derived hydrophobin protein (Scherrer et al. 2000, 2002; Scherrer & Honegger, 2003), the characteristic hydrophobic lining of aerial hyphae in the fungal kingdom which self-assembles at the liquid–air interface (Wösten et al. 1993; Wessels 1997; Wösten 2001). Despite being located in the thalline interior, the hyphae of the photobiont and medullary layers are aerial, their hydrophobin layer spreads over the wall surfaces of the photobiont cell population, thus sealing the apoplastic continuum with a hydrophobic coat (Fig. 6.4). The same happens in the lichenized basidiocarp of Dictyonema glabratum (syn. Cora pavonia; Trembley et al. 2002a, b). The mycobiont-derived hydrophobic wall surface layer plays a crucial role in the functioning of the symbiosis. In co-cultures under sterile conditions, hydrophobin protein is synthesized at an early stage of thallus resynthesis at the contact site of Usnea hakonensis and its chlorobiont (Trebouxia sp.; Kono et al. 2020).

A diagram depicts the gas-filled thalline interior, aerial hyphae with water-repellent wall surface layer, and conglutinate upper cortex, with 6 processes. The labeled parts are water, oxygen, carbon dioxide, carbohydrates, vapor, and nutrients. — **Fig. 6.4**

Traditionally, gas exchange of lichens was measured in the same way as in plant leaves, i.e., outside the thallus which is built up by the heterotrophic partner. However, CO₂ diffusion through the cortex is blocked in fully hydrated thalli; this was interpreted as a depression of photosynthesis at high moisture contents, and water was assumed to fill the intercellular space in the thalline interior (Lange and Tenhunen 1981). In ultrastructural studies, the hydrophobic lining of the wall surfaces in the algal and medullary layers was shown to prevent water from accumulating outside the apoplastic continuum, the algal and medullary layers being gas-filled at any level of hydration (Honegger 1991a, b). The mycobiont of macrolichens amounts to approx. 80% of thalline biomass, the photobiont cell population to approx. 20% or less. The cortex is translucent when wet, but opaque when dry, and chlorophyll fluorescence is highest in fully hydrated thalli. It was postulated that there should be enough mycobiont-derived respiratory CO₂ in the thalline interior to secure the photosynthetic activity of the photobiont in fully hydrated thalli (Honegger 1991a). By oximetric measurements of electron transport within thalli and fluorimetric measurements of photosynthesis in Flavoparmelia caperata and its Trebouxia chlorobiont, ten Veldhuis et al. (2019) showed that photosynthetic O₂ and photosynthates are taken up by the mycobiont and its respiratory CO₂ by the chlorobiont, the algal and fungal energy metabolism being mutually linked, a perfect recycling system.

4.5 Heavy Metal and Radionuclides

Lichens absorb not only water and nutrients, but also pollutants, heavy metals and radionuclides included. Thus, they are used in biomonitoring studies in urban and industrial areas (Nimis et al. 2002; Abas 2021). They have also been used as silent chronists of early nuclear weapon testing and of the Chernobyl and Fukushima accidents (Seaward 2002; Saniewski et al. 2020; Dohi et al. 2021; Anderson et al. 2022). Heavy metals are bound in insoluble complexes within the thallus. Characteristic lichen communities develop on heavy metal rich rock substrates. 5000 ppm of copper were found in the crustose thalli of Lecanora vinetorum: it grows on wooden supports in vineyards in South Tyrolia which, for decades, were sprayed 12 times per year with copper sulfate as a fungicide to protect the Vitis cultivars (Poelt and Huneck 1968); the mycobiont-derived xanthone vinetorin is assumed to form insoluble copper complexes.

5 The Microbiome of Lichen Thalli

5.1 The Bacteriome: Bacterial Epi- and Endobionts of Lichen Thalli

At least since the Early Devonian (approx. 415 Ma ago), non-photosynthetic bacteria live on the thallus surface of lichens, and filamentous actinobacteria are found on their cortex and in the thalline interior (Fig. 6.5a–b; Honegger et al. 2013b). In the twenty-first century, the taxonomic diversity and potential role of the bacteriome for lichen symbiosis was intensely explored, as reviewed by Grube and Berg (2009), Grube et al. (2012, 2016), and Grimm et al. (2021).

Ten images depict the past and present of epi and endolithic bacteria. The labeled measurements for images a to i is in micrometer 10, 25, 20, 5, 10, 10, 20, 1, and 5. — **Fig. 6.5**

Many lichens live in nutrient-poor habitats such as bare rock surfaces, steppe and desert or oligotrophic boreal-arctic ecosystems. Numerous plant-beneficial bacteria have been identified in the rhizosphere of plants (Burr et al. 1984; Davison 1988); some of them fix nitrogen, others solubilize phosphate or act as antagonists of plant pathogens and thus are important in sustainable agriculture (Romano et al. 2020). Considering the ubiquitous bacterial epi- and endobionts of lichen thalli (Fig. 6.5c–j), the question was: are there any lichen-beneficial bacteria (Honegger 1991b)? Maria Cengia Sambo (1924, 1926) was the first to culture and identify an Azobacter associated with lichens and referred to its potential role as a N₂-fixing partner; she introduced the term polysymbiosis. In the last decades, a whole range of nitrogen-fixing representatives of Rhizobiales and Frankia have been characterized as associates of lichen thalli (Hodkinson and Lutzoni 2009; Bates et al. 2011; Erlacher et al. 2015; Eymann et al. 2017; Almendras et al. 2018, etc.). Some lichen-associated Rhizobiales synthesize β-carotenes (Pankratov et al. 2020). The most common and widespread bacterial symbionts of lichens are representatives of Alphaproteobacteria. The bacterial community may change upon infection of the thallus by lichenicolous fungi or lichens (Wedin et al. 2016). Chlorolichens carry different bacterial communities than cyanolichens (Almendras et al. 2018).

In non-lichenized fungi, the intimate bacterial–fungal interaction triggers the biosynthesis of secondary metabolites such as archetypal polyketides in A. nidulans (Schroeckh et al. 2009) or a cryptic meroterpenoid pathway in A. fumigatus (König et al. 2013).

Comparative analyses of the bacteriome of lichens from different ecosystems were performed, e.g., the littoral (Sigurbjornsdottir et al. 2014; Parrot et al. 2015; West et al. 2018), high mountain areas such as alpine soil crust lichens (Muggia et al. 2013), the Andean Paramo (Sierra et al. 2020), the Qinghai–Tibet Plateau (Hei et al. 2021) or tropical rainforests (Mara et al. 2011). The best investigated is the microbiome of the lung lichen, Lobaria pulmonaria, as reviewed by Grimm et al. (2021).

In the desiccated state, i.e., in herbaria, some bacterial symbionts retain their viability for decades (Cernava et al. 2016), whereas lichen myco- and photobionts die off within a few years of storage at room temperature (Honegger 2003). Thus, herbaria with specimens from remote areas might be a source of interesting bacterial associates of lichens, some of them with biologically interesting properties (Cernava et al. 2016). In nature, bacterial associates of lichen thalli survive drought stress unharmed (Cernava et al. 2018).

Within thalli, the species richness and cell density of lichen-associated bacteria increase from peripheral, young growing zones to older, non-growing areas. In the lobate Xanthoparmelia, the highest bacterial diversity was found in the centre (Mushegian et al. 2011), in the fruticose reindeer lichen Cladonia arbuscula or in the podetia of Cladonia squamosa in basal parts (Cardinale et al. 2008; Noh et al. 2020; Fig. 6.5g–i); some of the bacterial associates of old thallus areas are likely involved in biodegradative processes.

Vertical transmission of the microbiome (except the Nostoc cyanobiont of cephalodia) via symbiotic propagules occurs in the lung lichen (Lobaria pulmonaria; Aschenbrenner et al. 2014); with high probability isidia and thallus fragments of most other species also carry at least part of the microbiome at their surface, but whether soredia with very hydrophobic surfaces (Fig. 6.3e) carry bacteria remains to be seen. Lichen-inhabiting invertebrates have their own bacteriome on their surfaces (Chasiri et al. 2015).

Lichen-associated bacteria have attracted considerable interest as potential producers of novel secondary compounds with biotechnological potential, the focus being on actinobacteria (González et al. 2005; Parrot et al. 2015, 2016a, b; Suzuki et al. 2016).

5.2 Lichenicolous Fungi

Approximately 2320 spp. of lichenicolous asco- and basidiomycetes have been described (Fig. 6.6); 2000 spp. are obligately, 62 spp. facultatively lichenicolous and 257 spp. are lichenicolous lichens (Diederich et al. 2018), new families, new genera and species being continuously described from ecosystems which had not been previously investigated. Examples are representatives of Pleostigmataceae and Melanina spp. among the Chaetothyriomycetidae in crustose lichens from subalpine areas (Muggia et al. 2021), or Crittendenia spp. lichenicolous representatives of Pucciniomycotina (Basidiomycota; Millanes et al. 2021). A well-preserved lichenicolous Lichenostigma sp., (Arthoniomycetes, Ascomycota) was found on fossil Ochrolechia sp. in palaeogene amber (approx. 24 Ma old; Kaasalainen et al. 2019).

Eight images depict the lichenicolous ascomycetes in c, e, f, g, h, and i and basidiomycetes in a, b, d, and j. The labeled measures are a. 1 centimeter. b, c, e. 0.5 millimeters. f, h. 1 millimeter. i, j. 0.2 millimeter. and g. 50 micrometer. — **Fig. 6.6**

Some lichenicolous fungi have a minor impact on their host (e.g. mycocalicialean Sphinctrina spp. on Pertusaria spp., Fig. 6.6e), others have a devastating effect, killing the fungal and photoautotrophic partner (e.g. the corticialean basidiomycetes Marchandiomyces aurantiacus and M. corallinus on Physcia and Parmelia spp.; Fig. 6.6b). Only a few lichen spp. regenerate after an attack by the athelialean basidiomycete Athelia arachnoidea (Fig. 6.6a), whose asexual state is Rhizoctonia carotae, a pathogen of carrots (Adams and Kropp 1996), but the free space created by the killing effect is soon occupied by fast-growing crustose taxa such as Biatora spp. (Motiejûnaitë and Jucevièienë 2005).

Several lichenicolous fungi stimulate, probably via secretion of hormones, gall formations in their hosts (Hawksworth and Honegger 1994). Examples are the verrucarialean Telogalla olivieri on Xanthoria parietina, or the parmeliacean Raesaenenia huuskonenii on Bryoria spp. (Fig. 6.6h–i). The characteristic galls of members of the Biatoropsis usnearum complex (Tremellales, Basidiomycota; Fig. 6.6d; Millanes et al. 2016a) on Usnea spp. are basidiomata of the parasite. Even hyperparasitism was detected (e.g. Tremella huuskonenii, parasite of R. huuskonenii on Bryoria sp., Fig. 6.6j; Lindgren et al. 2015).

Various investigators found basidiomycetous yeasts as symptomless endolichenic fungi on and in lichen thalli, belonging to the Tremellomycetes (Agaricomycotina), Cystobasidiomycetes or Agaricostilbomycetes (Pucciniomycotina; review: Diederich et al. 2018). Examples are Fellomyces spp. (Cuniculitremataceae, Tremellales; Prillinger et al. 1997; Lopandic et al. 2005), the Cyphobasidium usnicola complex and other Cyphobasidium spp. on various macrolichens (Cystobasidiales; Millanes et al. 2016b; Spribille et al. 2016), or Lichenozyma pisutiana in Cladonia spp. (Cystobasidiales; Černajová and Škaloud 2019). These basidiomycetous yeasts are widespread, but not ubiquitous in lichen thalli (Lendemer et al. 2019). Particularly interesting are tremellalean lichenicolous fungi which produce galls on their host lichen, but switch between a yeast and a hyphal stage, the former being located on and in the cortex of the lichen, as visualized with FISH (fluorescent in situ hybridization techniques; Spribille et al. 2016). Examples are Tremella lethariae on Letharia vulpina (Tuovinen et al. 2019), T. macrobasidiata and T. varia on Lecanora spp. (Tuovinen et al. 2021).

Some lichenicolous fungi reduce the growth rate and the production of secondary metabolites of their host (e.g. Plectocarpon spp. on Lobaria pulmonaria; Asplund et al. 2018; Merinero and Gauslaa 2018), others degrade the secondary metabolites of their host (e.g. parietin of Xanthoria parietina by the capnodialean Xanthoriicola physciae; Edwards et al. 2017, or lecanoric acid by hypocrealean Fusarium spp. on Lasallia spp.; Lawrey et al. 1999), thus facilitating the attack of opportunistic fungi and/or enhancing the grazing pressure by lichenivorous invertebrates (Lawrey et al. 1999; Asplund et al. 2016). More and different secondary metabolites than in the lichen proper were found in Cladonia foliacea upon infection with the lichenicolous Heterocephalacria bachmannii (Filobasidiales, Tremellomycetes), the antioxidant potential of the thallus being enhanced (Khadhri et al. 2019).

5.3 Lichenicolous Lichens

Lichenicolous lichens (Fig. 6.7a–c) are a group of specialists whose ascospore-derived germ tubes start their development in the thallus of a host lichen, which they invade; some of them take over the photobiont host, others acquire a different green algal partner (see below). The parasitic lichen overgrows its host and differentiates its own thallus. The first known lichenicolous lichen, Rhizocarpon lusitanicum, parasite of Pertusaria spp., was described by Nylander in 1865 when lichen symbiosis was not yet defined. In their 2018 compilation, Diederich et al. listed 257 spp. of lichenicolous lichens and their hosts, representatives of 63 genera, 28 families, 16 orders and four classes of ascomycetes. The vast majority are Lecanoromycetes, the most species-rich genera being Rhizocarpon (33 spp.), Acarospora (27 spp.) and Caloplaca (26 spp.; Diederich et al. 2018).

Three images depict lichenicolous lichens. a. Diploschistes muscorum overgrowing of ascomata. b. Caloplaca anchon-phoeniceon in 1 millimeter. c. Rihzocarpon effiguratum in 1 millimeter. — **Fig. 6.7**

The acquisition of the photobiont by the lichenicolous Diploschistes muscorum on Cladonia spp. was investigated using light microscopy techniques applied to symbiotic and cultured photobiont cells (Friedl 1987). In the first developmental stage on Cladonia sp., D. muscorum was shown to associate with Asterochloris irregularis (syn. Trebouxia irregularis), the unicellular green algal partner of the Cladonia host; subsequently algal switching occurred, A. irregularis being replaced by Trebouxia showmanii (Friedl 1987) and/or other Trebouxia spp. (Wedin et al. 2016). Diploschistes spp. associate with diverse photobiont species, as concluded from molecular investigations of D. diacapsis in Mediterranean soil crust communities, up to four different Trebouxia spp. having been found in one thallus (Moya et al. 2020).

5.4 Endolichenic Fungi (ELF)

Whereas the diversity of lichenicolous fungi has been intensely investigated from the nineteenth century onwards, the presence of numerous symptomless endolichenic fungi in lichen thalli was first detected towards the end of the twentieth century (Petrini et al. 1990). Today, more than 200 spp. of endolichenic fungi are known, predominantly ascomycetes, few basidio- and zygomycetes, 135 having been identified at species level; they were isolated from 114 lichen species, the majority being parmeliacean macrolichens (Chakarwarti et al. 2020).

Most ELF are saprobic generalists, but also several wood-decay asco- and basidiomycetes were found such as the xylarialean Xylaria, Hypoxylon and Daldinia spp., or the agaricales Schizophyllum commune and the russulales Heterobasidion annosum (Fig. 6.8). Lichen thalli as a refuge of wood-decay fungi: an unexpected result! Some ELF are plant pathogens, a few are also endophytes of plants (Arnold et al. 2009; U’Ren et al. 2010, 2012). The biology of endolichenic fungi is poorly investigated; they absorb polyols such as mycobiont-derived mannitol from the apoplastic continuum of the lichen thallus (Yoshino et al. 2020).

An image depicts the thin hyphae of endolichenic fungi growing between the medullary hyphae and the clamp connection of an endolichenic agaricomycetes. The label measures 10 micrometers. — **Fig. 6.8**

Upon isolation into sterile culture, ELF turned out to be a rich source of interesting bioactive secondary metabolites. More than 140 novel compounds have been identified, many of them with pharmaceutical potential such as antibiotic, antiviral, antifungal, anti-inflammatory, antiproliferative or antioxidant properties (reviews: Gao et al. 2016; Kellogg and Raja 2017; Tripathi and Joshi 2019; Agrawal et al. 2020; Wethalawe et al. 2021). Considering that only approximately 5% of lichen species have so far been investigated for ELF, there are lots of interesting work ahead.

5.5 The Virome of Lichens

Upon isolation into sterile culture, the first mycoviruses in the mycobiome of lichens were detected in the so-called dust lichens, i.e., the leprose thalli of Lepraria incana (Stereocaulaceae, Lecanoromycetes; LiCV1) and Chrysothrix chlorina (Chrysotrichaceae, Arthoniomycetes; CcCV1). LiCV1 and CcCV1 are classified in the genus Alphachrysovirus (family Chrysoviridae; Petrzik et al. 2019) whose host range comprises fungi, plants and possibly insects (Kotta-Loizou et al. 2020). Upon closer examination, i.e., with fluorescent in situ hybridization techniques, CcCV1 was located not in the lichen mycobiont proper, but in an associated Penicillium citreosulfuratum (Eurotiomycetes; Petrzik et al. 2019).

Lichen photobionts were shown to harbour plant viruses such as the cauliflower mosaic virus (Petrzik et al. 2013). With immunogold labelling techniques applied to ultrathin sections, viruses contained in more than 70 years old sterile cultures of Trebouxia aggregata, photobiont of Xanthoria parietina, were shown to be located in the algal cytoplasm, not in the chloroplast; upon mechanical transmission to plant host cells these phycobiont-derived viruses were infective (Petrzik et al. 2015).

In a study on virus diversity in the metagenome of the saxicolous Umbilicaria phaea, five novel viruses were detected, one of them, a Caulimovirus, being associated with the Trebouxia photobiont and the four others, belonging to the Myoviridae, Podoviridae and Siphoviridae, with bacterial associates of the lichen, but so far, no mycoviruses have been found (Merges et al. 2021).

RNA virus diversity was investigated in an extract of a microcosm, predominantly consisting of Cladonia spp. and other Lecanoromycetes and their trebouxiophycean photobionts, overgrowing bryophytes, non-lichenized ascomycetes, cyanobacteria, free-living green algae, fern (spores?) and minute animals living therein, as seen in SSU rRNA sequences (Urayama et al. 2020). A total of 65 operational taxonomic units (OTUs) were achieved, 17 belonging to Partitiviridae (five to the genus Alphapartitivirus, one to Betapartitivirus, the host range of both genera comprising fungi and plants; Vainio et al. 2018), plus representatives of 10 additional viral families and several unclassified dsRNA and ssRNA viruses (Urayama et al. 2020).

The impact of viral infections on the biology and whether horizontal virus transfers occur between the partners of lichen symbiosis and their allies remain to be investigated.

6 Fossil Lichens and Their Microbiome

6.1 Fossil vs. Extant Lichens

Fungi colonized terrestrial environments in the Proterozoic, presumably associating with the even more ancient cyanobacteria, the latter having been present already in the Archean (approx. 2400 Ma), but colonized terrestrial habitats from the Proterozoic onwards, as concluded from fossil records and molecular clock analyses (Strother and Wellman 2016; Lutzoni et al. 2018; Demoulin et al. 2019; Garcia-Pichel et al. 2019). Trebouxiophyceae, unicellular green algae, and Trentepohliales, filamentous green algae, were present from the Proterozoic onwards, some extant taxa of both groups being the main photobionts of extant LFF (Lutzoni et al. 2018; del Cortona et al. 2020). Thus, lichenization is assumed to be an ancient fungal lifestyle, but fossil records are very scarce and partly difficult to interpret (Fig. 6.9).

A schematic is processed in 4 steps. 1. Proterozoic of Neoproterozoic, 1 label parts. 2. Paleozoic of cam, ord, sil, dev, carb, and perm, 6 label parts. 3. Mesozoic of tri, jur, and cretac, 3 label parts. 4. Centoz of paleo, 3 label parts. — **Fig. 6.9**

According to molecular phylogenetic datasets, the clades of ascomycetes which gave rise to extant lichens did not radiate before the Silurian (approx. 450 Ma; Lutzoni et al. 2018) or even the Mesozoic (approx. 250 Ma; Nelsen et al. 2019). According to the latter authors ascolichens, as we know them today, are younger than previously assumed, did not predate the evolution of vascular plants and were not among the (extinct) early fungal colonizers of terrestrial habitats. Nevertheless, the lichen lifestyle was most likely established in the common and widespread nematophytes and Prototaxites spp. (review: Selosse and Strullu-Derrien 2015). The manyfold problems related to the interpretation of fungal fossils are summarized by Berbee et al. (2020).

6.2 Palaeozoic Fossils

An approx. 600 Ma old lichen-like association was preserved in marine phosphorite of the Doushantuo Formation in South China (Yuan et al. 2005). Mats of cyanobacterial or coccoidal algal cells were invaded by extremely thin filamentous hyphae with diameters below 1 micron, a characteristic feature of actinobacteria, not fungi (Honegger 2018); thus, the Doushantuo fossils are not lichens.

Nematophytes, an extinct phylum of presumably lichenized fungi with no modern analogues and thus not represented in molecular phylogenetic trees of living species, were common and widespread constituents of terrestrial cryptogamic ground covers from the late Silurian to the late Devonian. They comprise the families Nematothallaceae (genera Nematothallus, Cosmochlaina, Tristratothallus; Edwards et al. 2013, 2018) and Nematophytaceae (genera Nematoplexus, Nematasketum and the enigmatic Prototaxites; Edwards and Axe 2012). After long debates about their taxonomic affiliation nematophytes are currently interpreted as presumably lichenized thalloid fungal structures (Edwards et al. 2013, 2018). Cross-fractures of some nematophyte fossils reveal the same stratification as found in lichens, with a conglutinate peripheral cortex and a medullary layer built up by interwoven hyphae, but photobiont cells are missing; they might have been lost during fossilization. In charcoalifying experiments with extant cyanobacterial lichens, the fungal partner was well preserved, and so were the thick mucilaginous sheaths of the Nostoc photobiont, but most of the cyanobacterial cells proper were lost (Honegger et al. 2013a).

Prototaxites spp., enigmatic fossils with erect axes, built up by hyphae of various diameters, ranging from pencil size dimensions as in the mid-Ordovician (Darrivilian, approx. 460 Ma old) P. honeggeri (Retallack 2020) to more than 8 metres long stems, as in the mid-Devonian (early Givetian, approx. 385 Ma old) P. loganii, were interpreted as presumably lichenized fungi, coccoid photobiont cells having been resolved at the surface of the axes of both species (Retallack and Landing 2014; Retallack 2020). However, it remains unclear how the few coccoid algal cells should have provided enough carbohydrate to nourish these large fungal structures; nematophytes were assumed to be associated with Prototaxites (Selosse and Strullu-Derrien 2015). Delicate fruiting structures at the surface of the axes were seldom retained; luckily the hymenial layer was preserved in a series of petrographic thin sections of P. taiti of the Kidston and Lang collection. The ascomata of P. taiti combine features of extant ascomycetes, i.e., Taphrinomycotina (Neolectomycetes lacking croziers) and Pezizomycotina (epihymenial layer secreted by paraphyses), but Prototaxites is not an ancestor of the latter (Honegger et al. 2018).

The mid-Devonian Spongiophyton minutissimum is a presumed lichen, built up by a conglutinate, tissue-like, porate fungal cortex around a central cavity; a photobiont was not resolved (Taylor et al. 2004).

Winfrenatia reticulata is a permineralized fossil lichen, 10 cm long, 2 mm thick, from the Lower Devonian Rhynie chert (approx. 400 Ma old; Taylor et al. 1995, 1997). A presumed mucormycete forms a basal mat and superimposed ridges built up by parallel hyphae which are in contact with coccoid cyanobacterial cells interspersed with a filamentous cyanobacterium (Karatygin et al. 2009). However, Winfrenatia might be a fragment of a larger thalloid organism such as a nematophyte (Honegger, unpubl.).

The oldest lichenized ascomycetes with dorsiventally organized, internally stratified thallus so far found are charcoalified fragments of Cyanolichenomycites devonicus, a cyanobacterial lichen with Nostoc-like photobiont (Fig. 6.10a, b), and Chlorolichenomycites salopensis, a presumed green algal lichen whose globular photobiont cells were retained as framboidal pyrite (Fig. 6.10c–e; Honegger et al. 2013a). Both fossils were extracted from a Lower Devonian siltstone from the Welsh Borderland (approx. 415 Ma old). Despite their striking structural similarity with extant Lecanoromycetes lichens, the taxonomic affiliation of these fossils remains unclear. They might either belong to the nematophytes or represent the earliest known members of extant lichenized ascomycetes (Hawksworth 2012; Lutzoni et al. 2018); in the latter case, some molecular clock estimates would require recalibration.

Five images depict the fossil lichens from the lower Devonian in comparison with lecanoromycetes, where images a and b are well-preserved with gelatinous sheaths. The label measures 20, 10, and 25 micrometers. — **Fig. 6.10**

6.3 Mesozoic Fossils

Daohugouthallus ciliiferus, a well-preserved, band-shaped lichen resembling extant Parmeliaceae such as Pseudevernia furfuracea, was found in mid Jurassic sediments (approx. 165 Ma old) in north-eastern China (Inner Mongolia; Wang et al. 2010; Fang et al. 2020).

Very well preserved is the Mesozoic Honeggeriella complexa, a dorsiventrally organized, foliose lichen from the Early Cretaceous of Vancouver Island (Valanginian-Hauterivian boundary, ca. 133 Ma old) with distinct green algal layer and haustorial complexes at the mycobiont–photobiont interface comparable to those found in extant taxa (Matsunaga et al. 2013).

6.4 Cenozoic Fossils

Large numbers of well-preserved lichens were found in Cenozoic Baltic and Bitterfeld (approx. 50–35 Ma old) and in Dominican amber (approx. 16 Ma old). Excellent external and internal structural preservation allows to identify taxa similar or closely related to extant species (Hartl et al. 2015), most of them having been epiphytes on the resin-producing trees (e.g. Pinus spp. in N-Europe). Among the fruticose-pendulous lichens in Baltic amber are alectorioid taxa and Usnea spp. (Kaasalainen et al. 2015, 2020). Among the foliose lichens is Anzia electra, common and widespread in Baltic and Bitterfeld amber, but today extinct in Europe (Rikkinen and Poinar 2002; Schmidt et al. 2013). Very well preserved Parmelia ambra and P. isidiiveteris (Poinar Jr. et al. 2000) and Phyllopsora dominicanus (Rikkinen and Poinar 2008) were found in Dominican amber. Among the crustose lichens in Baltic amber are calicioid taxa (Rikkinen 2003; Rikkinen et al. 2018) and Ochrolechia spp. (Kaasalainen et al. 2019).

There are many more types of amber worldwide whose fossils await thorough investigation, the oldest ones dating back to the Carboniferous period (approx. 320 Ma old). DNA has been successfully extracted, amplified and sequenced from invertebrate and plant fossils in Dominican and Lebanese amber, the oldest ones being approx. 120–135 Ma old (Poinar 1994).

6.5 The Microbiome of Fossil Lichens

In the dorsiventrally organized thallus of the Lower Devonian Chlorolichenomycites salopensis were bacterial colonies growing on the surface of the cortex and actinobacteria and lichenicolous fungi in the thalline interior, comparable to the situation in extant lichens (Fig. 6.5a, b; Honegger et al. 2013b).

Fructifications of Lichenostigma sp. (Lichenostigmatales, Arthoniomycetes) were found on Ochrolechia sp. in palaeozoic amber (Kaasalainen et al. 2019), Lichenostigma spp. being common and widespread lichenicolous fungi of extant lichens (Hafellner and Calatayud 1999; Diederich et al. 2018). A wide range of filamentous fungi were found on decaying crustose lichens embedded in amber, such as well-preserved toruloid taxa, conidiomata of dematiaceous hyphomycetes resembling extant genera such as Sporidesmium, Taeniolella and Taeniolina (Kettunen et al. 2016, 2018).

7 Lichen–Animal Relations

7.1 The Micro- and Mesofauna of Lichen Thalli

Many interactions of lichens with protozoans, invertebrates and vertebrates have been reported. Among lichen–invertebrate interactions are rotifera, amoebae (Figs. 6.1a, b and 6.11a), ciliates, tardigrades (Fig. 6.11b), mites (Fig. 6.12a, b), spiders, nematodes, collembola and insects (springtails, barklice, lepidopterans, grasshoppers, etc.) which live between and below, some even within lichen thalli (reviews: Gerson 1973; Gerson and Seaward 1977; Sharnoff 1998; Segerer 2009). Epiphytic lichen biomass on oak correlated significantly with the abundance of arthropods, tardigrades and rotifera in central Maine (Stubbs 1989). The microfauna of one lichen species (Xanthoria parietina), collected in Lithuania, comprised 16 protozoan taxa, three tardigrades, two Nemathelminthes and three rotifera (Šatkauskienė 2012). In 26 terricolous lichen samples from Svalbard and Spitzbergen, 23 species of tardigrades were identified (Zawierucha et al. 2017). On Cladonia rei growing on heavy metal-contaminated post-smelting dumps in Poland, 50 species of oribatid mites were recorded (Skubała et al. 2014).

Two diagrams depict the microfauna of lichen thalli. a. Testate amoeba with agglutinate shell,. b. Tardigrade on the surface of a campylidum. The label measures for a and b is 10 micrometer. — **Fig. 6.11**

Six images depict the lichenivory and endozoochory in oribatid mites. The label measures are a and b. 0.1 millimeters. c. 0.5 millimeters. d and g. 1 millimeters. f. 50 micrometer. — **Fig. 6.12**

Some of these allies of lichen thalli find shelter, others are lichenivorous (see below) or bacterivorous (Liu et al. 2011). Even pest insects of fruit and nut trees find shelter under epiphytic lichens; therefore, agricultural experts recommend fruit growers to control or even prevent lichen growth either mechanically or chemically in their orchards.

7.2 Lichenivory: Invertebrates

Lichens have always been part of terrestrial food webs. The Silurian-Devonian nematophytes, presumably lichenized fungi, were grazed by arthropods, presumably millipedes, as seen in grazing marks on the thallus surface with adhering coprolites (fossil faecal pellets), some of which contain hyphae or even small fragmentary remains of the thalli (Edwards et al. 1995, 2020). Grazing marks, presumably from arthropods, and faecal pellets were found on fossil foliose lichens in Palaeogene Bitterfeld amber (Schmidt et al. 2022).

There is a large body of literature on lichenivorous invertebrates (Gerson and Seaward 1977; Rambold 1985; Sharnoff 1998; Segerer 2009). In feeding experiments, Arthropoda such as mites (Acari), springtails (Collembola), barklice (Psocoptera) or beetles (Coleoptera) and Gastropoda such as door and pillar snails (Clausiliidae, Cochliopsidae) were all shown to graze the upper cortex and algal layer of Parmelia and Physcia spp. down to the medullary layer (Schmidt et al. 2022). Lichens were assumed to be protected from lichenivory by their content in secondary metabolites (Stahl 1904). However, many invertebrates consume even those parts of lichen thalli which contain large amounts of secondary products unharmed, crystals of these fungal metabolites passing the digestive tract unchanged (Zopf 1907; Hesbacher et al. 1995; Asplund and Wardle 2013; Gadea et al. 2019). Lichenivorous mites are selective in their food choice, some lichen species being avoided (Reutimann and Scheidegger 1987; Fröberg et al. 2003). In molluscs (slugs and snails), a preference was noted for thallus areas or even species with low contents in secondary metabolites (Benesperi and Tretiach 2004; Asplund 2011). Arion fuscus preferentially feeds on the large internal cephalodia of Nephroma arcticum, probably because these lack secondary metabolites (Asplund 2010; Asplund and Gauslaa 2010). Feeding experiments with thalli whose secondary products had been removed by rinsing in acetone were preferentially grazed (Gauslaa 2005; Boch et al. 2011, 2015). Gall-producing lichenicolous fungi (Plectocarpon spp.) reduce the growth rate and the production of secondary metabolites in Lobaria pulmonaria (Asplund et al. 2016; Merinero and Gauslaa 2018), thus making the infected thallus areas more palatable and increasing the grazing pressure by snails (Asplund et al. 2016).

7.3 Lichenivory: Vertebrates

No vertebrate lives exclusively on a lichen diet, but in many regions, lichens are a substantial part of total food intake when other, preferred food such as buds, leaves, tubers and fruits are seasonally unavailable. Mat-forming terrestrial lichens such as Cladonia spp., and epiphytic species are a substantial part of the diet of reindeers and caribou (Rangifer tarandus) in Arctic tundras (Heggberget et al. 2002), but also of other ungulates such as deer, chamois or alpine Ibex in montane and alpine ecosystems of the Northern and Southern Hemisphere (Parrini et al. 2009; Yockney and Hickling 2000), of camelids (guanacos, llamas) in South America (Follmann 1964) and of numerous smaller mammals such as marmots, flying squirrels (Rosentreter et al. 1997), voles, etc. (reviews: Richardson and Young 1977; Sharnoff and Rosentreter 1998; Segerer 2009). Trampling damage occurs in reindeer lichen stands in subarctic and arctic tundras when large herds are feeding in dry weather; reindeer lichens (Cladonia spp.), like all other lichens, are elastic and flexible when wet, but very brittle in the dry state, thus being fragmented by the hooves of ungulates, recovery taking more than 30 years (Pegau 1970; den Herder et al. 2003; Théau et al. 2005; Heggenes et al. 2017, 2020).

However, trampling damage and overgrazing are not the only reasons for the decline of lichen heaths in Arctic ecosystems. In response to global warming, the Arctic is greening, deciduous shrubs and graminoids increasingly outcompete the terricolous lichen communities, as observed in situ and with remote sensing technologies over time (Myers-Smith et al. 2011, 2019; Fraser et al. 2014; Aartsma et al. 2020; Berner et al. 2020). Increasing summertime temperatures are also causing the decline of cyanobacterial and other lichens in soil crust communities on the Colorado Plateau, where neither grazing nor anthropogenic disturbances are evident (Finger-Higgens et al. 2022).

Large quantities, i.e., 30–75% of total food intake of beard lichens, especially Usnea longissima and Bryoria spp., are consumed by colobine primates (snub-nosed monkeys; Fig. 6.13) of the genus Rhinopithecus (R. bieti, R. roxellana, R. brelichii) in Western China and adjacent Tibetan mountain areas (Xiang et al. 2007; Grueter et al. 2009, 2012; Li and Ang 2009; Kirkpatrick and Grueter 2010; Liu et al. 2013; Bissell 2014; Xiang 2014). The rare and endangered lowland R. strykeri was shown to eat 15 lichen spp. in captivity, but these amounted to less than 3% of his diet (Yang et al. 2019). Barbary macaques (Macaca sylvanus) in high-altitude fir forests in the Ghomaran Rif and other mountain areas in Marocco eat lichens only in harsh winters when no other food is available (Mehlman 1988).

A photograph of the Yunnan black snub-nosed monkey feeding on usnea longissima under the branch of the tree. — **Fig. 6.13**

Lichens are rich in easily digestible carbohydrates such as β-glucans in the fungal cell walls such as lichenin (Honegger & Haisch, 2001) but have only low protein content. Reindeer and caribou seasonally feed on mushrooms (Inga 2007), whereas colobines consume mushrooms, invertebrates (Xiang et al. 2007; Yang et al. 2016) and vertebrates such as flying squirrels or bird’s eggs (Grueter et al. 2009), and even infanticide followed by cannibalism was observed (Xiang and Grueter 2007).

7.4 Endozoochory

Faecal pellets of lichenivorous invertebrates are probably common and widespread symbiotic propagules, but rarely described and experimentally investigated. Jahns (1987) reported on a novel type of symbiotic propagule in Solorina crocea but did not realize that these were germinating faecal pellets of lichenivorous snails. In light microscopy studies, numerous investigators observed intact fungal and/or algal cells or thallus fragments in the intestines or faecal pellets of lichenivorous invertebrates, e.g., in oribatid mites (Acari; Lawrey 1980; Meier et al. 2002), springtails (Collembola; Lawrey 1980), butterfly larvae (Lepidoptera; Rambold 1985; Brodo et al. 2021), termites (Termitidae; Barbosa-Silva and Vasconcellos 2019; Barbosa-Silva et al. 2019b), and molluscs (snails and slugs, Gastropoda; Baur et al. 2000; Fröberg et al. 2001; Boch et al. 2011, 2015).

However, in only a few lichen–invertebrate interactions was the viability of the cells contained in faecal pellets tested with culturing experiments. Gut transmission of viable mycobiont and photobiont cells was found in oribatid mites which had been feeding on Xanthoria parietina (Fig. 6.12a–g); the identity of both partners in these cultures was identified with molecular tools (Meier et al. 2002). Physcia adscendens and Lobaria pulmonaria were fed to nine gastropod species and the regeneration rate out of their faecal pellets tested. To a varying percentage, P. adscendens grew out of the faeces of all nine gastropod species (9/9), L. pulmonaria out of eight (8/9; Boch et al. 2011, 2015). No germination was observed in faecal pellets of lichenivorous snails and barklice which had been feeding on foliicolous lichens in a tropical rainforest (Lücking and Bernecker-Lücking 2000).

Various investigators report on partly severe grazing damage in saxicolous and epiphytic lichen communities (e.g. Baur et al. 1995, 2000; Gauslaa et al. 2006; Skinner 2021), but considering the high regeneration rates of lichens out of detached thallus fragments and faecal pellets of lichenivorous invertebrates, there is also a potential for rejuvenation which deserves investigation.

7.5 Epizoochory

Epizoochory is probably a very common and widespread mode of dispersal of symbiotic propagules, thallus fragments or faecal pellets of lichenivorous invertebrates, but only few investigations have been published. Only few viable cells of the mycobiont and photobiont are required for regenerating a new thallus. Three types of epizoochory can be distinguished:

1.
Lichens growing on animals (invertebrates and vertebrates). Examples are (a) limpets (Patella spp., Mollusca) and barnacles (Cirripedia) in the littoral fringe whose calcareous shell is inhabited by Pyrenocollema halodytes (syn. Arthroprenia halodytes, Collemopsidium h.) and its cyanobacterial photobiont (Hyella caespitosa; see Fig. 15.1a in Honegger 2012). (b) foliose lichens growing together with fungi, algae and liverworts on the back of large weevils of the genus Gymnopholus in New Guinea (Gressitt et al. 1965; Gressitt 1966), which are getting several years old, as concluded from the lichen growth on their back (Gressitt 1970, 1977). This epizoic cryptogamic community is inhabited by mites, rotifers and nematodes; even a new family, genus and species of oribatid mites (Symbioribatidae, Symbioribates papuensis) were discovered which live among the cryptogams on the weevils’ back (Aoki 1966). Liverworts, lichens and fungi were also found growing on Costa Rican Shield Mantis (Choeradodis spp., Mantodea; Lücking et al. 2010). (c) lichens growing on the shell of some, but by far not all Giant Tortoises (Geochelone elephantopus) in Galapagos (Hendrickson and Weber 1964).
2.
Lichens being actively sampled for nesting or camouflage. Vertebrates: (a) Many birds such as hummingbirds, chaffinks, etc., use lichens for camouflage of their nest, which then seem to be part of the branch on which it is positioned; ideally these lichens continue to grow on the surface of the nest (Graves and Dal Forno 2018). On branches without lichen cover, fragments of bright-grey lichens on the surface of birds nests reflect light, concealment by light reflection being an important mode of camouflage (Hansell 1996). (b) Flying squirrels (Glaucomys sabrinus) use lichens as nesting material and food, soft Bryoria spp., having low contents of secondary metabolites, are preferentially collected (Rosentreter and Eslick 1993; Hayward and Rosentreter 1994).

Invertebrates: (a) Larvae of bagworms (Psychidae, Lepidoptera) mount tiny fragments of the lichens on which they feed to their silk bag as a very efficient camouflage (McDonogh 1939; see Fig. 16.16a, b in Honegger 2009). (b) Barklice cover the body of their nymph with minute fragments of lichens, algae and sand granules (Henderson and Hackett 1986), and so do the larvae of the green lacewing (Nodita pavida; syn.), which become invisible under their load of tiny lichen fragments (Slocum and Lawrey 1976). (c) Several species of lichenivorous, terrestrial snails of the genus Napaeus (Gastropoda, Pulmonata) actively paste fragments of lichens to their shell (Allgaier 2007; Holyoak et al. 2011).
3.
Passive sampling. Soredia, isidia and other symbiotic propagules, tiny thallus fragments or faecal pellets adhere to animal or human vectors and thus get dispersed. Examples are (a) mites carrying soredia (Stubbs 1995). (b) lichenivorous termites most likely carry fragments of lichens to their nest where a species-rich lichen community develops (Aptroot and Cáceres 2014; Barbosa-Silva et al. 2019a). (c) Woodpeckers are neither lichenivorous nor do they collect lichens for camouflage or nest building, but were found to carry vegetative propagules of lichens on their feet, chest and tail feathers in samples in a Finnish Natural History Museum (Johansson et al. 2021). (d) humans carry propagules or fragments of lichens on their clothes, as first described in cases of woodcutters disease, an allergic reaction to usnic acid containing lichens, in housewives in contact with their husbands clothes (Mitchell and Champion 1965; Aalto-Korte et al. 2005). The load of plant seeds, moss and lichen propagules on clothes of visitors of the Antarctic was thoroughly investigated, largest amounts having been found on socks of field working scientists (Huiskes et al. 2014). However, most of these lichen propagules on human clothes likely end up in the washing machine rather than invading Antarctic ecosystems.

Long-distance anthropogenic dispersal of epiphytic lichens on economic or ornamental plants is probably quite common (Bailey 1976). An example is Xanthoria parietina, which was not native to Australia, but is now growing around wineries in the Barossa Valley and elsewhere. In comparative RAPD-analyses of sterile cultured isolates of the mycobiont, some of the isolates from Australia and New Zealand clustered with those from southern France and Spain (Honegger et al. 2004a, b). It could be that X. parietina was brought to these areas with plants or cuttings of grape wine (Vitis vinifera). Similarly, Brodo et al. (2021) concluded that X. parietina was anthropogenically transported from coastal to inland areas in Canada, presumably with trees from nurseries.

8 Lichenomimesis

8.1 Lichenomimesis in Animals

Large numbers of invertebrates mimick lichens and are thus not easily detected by potential predators (Figs. 6.14a–e). The earliest report of lichenomimesis in insects is a moth lacewing, Lichenipolystoechotes angustimaculatus (Neuroptera, Ithonidae), co-occurring with the mesozoic Daohugouthallus ciliiferus, which beautifully mimicked the pattern of the lichen on its wings (Fang et al. 2020). Extant examples are (1) lichen moths (Arctiinae, Lepidoptera) in their caterpillar (e.g. Catocala ilia; Fig. 6.14c) and/or adult stage such as Cleorodes lichenaria, the Brussels lace moth, whose lichenivorous caterpillar and moth stage mimick epiphytic lichens; (2) various species of bush crickets (Tettigoniidae, also termed katydids, in the genera Lichenomorphus, Lichenodracula, Markia, etc.; Braun 2011; Cadena-Castañeda 2011, 2013; Fig. 6.14a); one of them, Anapolisia maculata, even mimics foliicolous lichens in a tropical rainforest (Fig. 6.14b; Lücking and Cáceres 2002). (3) stick insects (Phasmatidae, syn. Phasmidae, such as Extatosoma tiaratum), or (4) spiders such as the North American Giant Lichen Orb Weaver (Araneus bicentenarius; Fig. 6.14d).

Four photographs of insects, spiders, and katydids. a. Nymphs of lichenodraculus matti. b. Anapolisia maculata mimicking. c. Caterpillar of the llia. d. Giant lichen orb spider. — **Fig. 6.14**

Among vertebrates, many frogs mimic lichens, such as the N-American Dryophytes versicolor (syn. Hyla versicolor), the Brazilian Bokermannohyla pseudopseudis (Leite et al. 2012) or the Australian tree frog Litoria genimaculata (Vanderduys 2012); the colouration may vary depending on the habitat. Foliicolous lichen communities are mimicked by tree frogs in Tanzanian (Leptopelis ulugurensis; Farkas and Pocs 1989) and S-American rainforests (Boana rufitela, syn. Hyla rufitela; Lücking and Cáceres 2002). Lichenomimesis occurs also in reptiles such as Rhampholeon spinosus (Chamaeleonidae) or Uroplatus sikorae and other Uroplatus spp. (Gekkonidae).

8.2 Lichenomimesis in Members of the Araceae (Flowering Plants)

A unique type of lichenomimesis occurs in petioles (leaf stalks) of some members of the Arum family (Araceae, monocotyledonous flowering plants). Representatives of several genera have spots on their petioles which resemble lichens (Fig. 6.15a–f); particularly interesting are Amorphophallus spp. (Barthlott 1995; Hejnowicz and Barthlott 2005; Claudel et al. 2019), among others A. gigas, the Giant Arum, which forms the largest inflorescence in the plant kingdom. One giant leaf per growing season grows out of the large tuber of these Araceae; it is fleshy and thus the vulnerable petiole resembles the stem of a lichen-covered tree, various types of crustose lichens being mimicked (Figs. 6.15a–f). This optical signal is obviously perceived by potential herbivores which assume these leaf stalks to be inedible wooden stems. Lichenomimesis is also seen in other Araceae such as Typhonium venosum (voodoo lily; Fig. 6.15f). The inflorescences of these Araceae emit a remarkable scent, reminiscent of decaying meat, partly intermixed with dung (e.g. horsedung in T. venosum), which attracts copro-necrophagous insects, some of them acting as pollinators (Claudel 2021). These plants of the Arum family successfully mimic elements of the fungal (i.e. lichens) and of the animal kingdoms.

Six images depict the pattern mimicking crustose lichens and their botanical names. — **Fig. 6.15**

9 Conclusions and Outlook

Molecular genetics have revolutionized our view on the biodiversity of LFF, their photobionts and their microbial associates. These investigations will continue at a global scale.

Lots of fossils, lichens and lichen-like organisms, from the Palaeozoic to the Cenozoic await thorough investigation.

The search for bioactive compounds, as produced by lichen-forming and endolichenic fungi and their bacterial associates will be intensified, several promising components having already been found. Examples are (1) usnic acid with antimicrobial, antiproliferative and antiviral properties (Macedo et al. 2021), as produced by various representatives of the Parmeliaceae in the lichenized and axenically cultured state (Yamamoto et al. 1985; Stocker-Wörgötter et al. 2013; Xu et al. 2022) and by endolichenic Streptomyces cyaneofuscatus (Parrot et al. 2016a); (2) antiproliferative cyaneodimycin from the same isolate of S. cyaneofuscatus (Parrot et al. 2016a) or (3) uncialamycin, a potent antibiotic with antiproliferative activity produced by Streptomyces uncialis, an endolichenic actinobacterium in Cladonia uncialis (Nicolaou et al. 2007, 2021; Parrot et al. 2016b). It will be interesting to see whether some of these products with pharmaceutical potential will reach the clinical trial phases. The large-scale production of mycobiont-derived secondary metabolites, either by heterologous expression in fast-growing fungi or by chemical synthesis, will be a challenge. S. uncialis-derived uncialamycin is chemically synthesized (Nicolaou et al. 2007).

Many bacterial associates of lichen thalli are in close contact with mycobiont-derived secondary metabolites with antibiotic properties, and some bacterial associates of lichens were shown to synthesize antibiotics (review: Grimm et al. 2021); an example is Streptomyces cyaneofuscatus, producer of usnic acid, which was isolated from the marine lichen Lichina confinis which does not synthesize usnic acid (Parrot et al. 2016a). The biotransformation of usnic acid into a compound with lower antibiotic activity was observed in several lichen-associated bacteria (Noël et al. 2021). The question is: are some of the epi- and endolichenic bacteria resistant to antibiotics? Bacterial antibiotic resistance emerged in the pre-antibiotic era; an example is the co-evolutionary adaptation of methicillin-resistant Staphylococcus aureus on hedgehogs whose skin is infected with antibiotic producing dermatophytes (Larsen et al. 2022).

Lichen-invertebrate and -vertebrate interactions deserve a closer examination as regards the dispersal of lichens and their allies. It would be interesting to see what birds carry on their feet and feathers in terms of symbiotic propagules (soredia, isidia, blastidia) or minute thallus fragments as well as faecal pellets of lichenivorous invertebrates or the minute lichenivorous mites proper. Examining the load of lichen propagules on the feathers and feet of birds with annual bipolar migration such as South Polar Skuas (Catharacta maccormicki, syn. Stercorarius m.) or Arctic Terns (Sterna paradisaea), which are assumed to be vectors of lichens with bipolar distribution (review: Garrido-Benavent and Pérez-Ortega 2017), would be particularly interesting. But also lichen dispersal by smaller birds, which are regularly landing on lichen-covered surfaces, should be investigated, for example, in collaboration with ornithologists during their ringing activities (Bailey and James 1979).

To conclude: there are lots of interesting work ahead, both in the field and laboratory.

References

Aalto-Korte K, Lauerma A, Alanko K (2005) Occupational allergic contact dermatitis from lichens in present-day Finland. Contact Dermatitis 52(1):36–38. https://doi.org/10.1111/j.0105-1873
Article Google Scholar
Aartsma P, Asplund J, Odland A, Reinhardt S, Renssen H (2020) Surface albedo of alpine lichen heaths and shrub vegetation. Arct Antarct Alp Res 52(1):312–322. https://doi.org/10.1080/15230430.2020.1778890
Article Google Scholar
Abas A (2021) A systematic review on biomonitoring using lichen as the biological indicator: a decade of practices, progress and challenges. Ecol Indic 121(article Nr. 107197):11. doi:https://doi.org/10.1016/j.ecolind.2020.107197
Adams GC, Kropp BR (1996) Athelia arachnoidea, the sexual state of Rhizoctonia carotae, a pathogen of carrot in cold storage. Mycologia 88(3):459–472. https://doi.org/10.2307/3760886
Article CAS Google Scholar
Agrawal S, Deshmukh SK, Reddy MS, Prasad R, Goel M (2020) Endolichenic fungi: A hidden source of bioactive metabolites. S Afr J Bot 134:163–186. https://doi.org/10.1016/j.sajb.2019.12.008
Article CAS Google Scholar
Ahmadjian V (1959) A contribution toward lichen synthesis. Mycologia 51(1):56–60. https://doi.org/10.2307/3755937
Article Google Scholar
Ahmadjian V (1962) Investigations on lichen synthesis. Am J Bot 49:277–283
Article Google Scholar
Allen JL, McMullin RT, Wiersma YF, Scheidegger C (2021) Population genetics and biogeography of the lungwort lichen in North America support distinct Eastern and Western gene pools. Am J Bot 108(12):2416–2424. https://doi.org/10.1002/ajb2.1774
Article CAS Google Scholar
Allgaier C (2007) Active camouflage with lichens in a terrestrial snail, Napaeus (N.) barquini Alonso and Ibáñez, 2006 (Gastropoda, Pulmonata, Enidae). Zool Sci 24:869–876
Article Google Scholar
Almendras K, García J, Carú M, Orlando JL (2018) Nitrogen-fixing bacteria associated with Peltigera cyanolichens and Cladonia chlorolichens. Molecules 23(12, article 3077):16. doi: https://doi.org/10.3390/molecules23123077
Altermann S, Leavitt SD, Goward T (2016) Tidying up the genus Letharia: introducing L. lupina sp. nov. and a new circumscription for L. columbiana. Lichenologist 48(5):423–439. https://doi.org/10.1017/S0024282916000396
Article Google Scholar
Ament-Velásquez SL, Tuovinen V, Bergström L, et al. (2021) The plot thickens: Haploid and triploid-like thalli, hybridization, and biased mating type ratios in Letharia. Front Fungal Biol 2 (Article 656386):19. doi:https://doi.org/10.3389/ffunb.2021.656386
Anderson J, Lévesque N, Caron F, Beckett P, Spiers GA (2022) A review on the use of lichens as a biomonitoring tool for environmental radioactivity. J Environ Radioact 243(3, article Nr. 106797):23. doi: https://doi.org/10.1016/j.jenvrad.2021.106797
Aoki J (1966) Epizoic symbiosis: an oribatid mite, Symbioribates papuensis representing a new family, from cryptogamic plants growing on backs of Papuan weevils (Acari: Cryptostigmata). Pac Insects 8:281–289
Google Scholar
Aptroot A, Cáceres M (2014) New lichen species from termite nests in rainforest in Brazilian Rondônia and adjacent Amazonas. Lichenologist 46(3):365. https://doi.org/10.1017/S0024282913000340
Article Google Scholar
Armaleo D, Sun X, Culberson C (2011) Insights from the first putative biosynthetic gene cluster for a lichen depside and depsidone. Mycologia 103(4):741–754
Article CAS Google Scholar
Arnold AE, Miadlikowska J, Higgins KL et al (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58(3):283–297. https://doi.org/10.1093/sysbio/syp001
Article Google Scholar
Asahina Y, Shibata S (1954) Chemistry of Lichen substances. Japan Society for the Promotion of Science, Tokyo
Google Scholar
Aschenbrenner IA, Cardinale M, Berg G, Grube M (2014) Microbial cargo: Do bacteria on symbiotic propagules reinforce the microbiome of lichens? Environ Microbiol 16(12):3743–3752. https://doi.org/10.1111/1462-2920.12658
Article CAS Google Scholar
Asplund J (2010) Lichen-gastropod interactions: chemical defence and ecological consequences of lichenivory. PhD thesis, Norwegian University of Life Sciences, Ås, 45 p. http://hdl.handle.net/11250/2429655
Asplund J (2011) Snails avoid the medulla of Lobaria pulmonaria and L. scrobiculata due to presence of secondary compounds. Fungal Ecol 4(5):356–358. https://doi.org/10.1016/j.funeco.2011.05.002
Article Google Scholar
Asplund J, Gauslaa Y (2010) The gastropod Arion fuscus prefers cyanobacterial to green algal parts of the tripartite lichen Nephroma arcticum due to low chemical defence. Lichenologist 42(1):113–117. https://doi.org/10.1017/S0024282909990284
Article Google Scholar
Asplund J, Wardle DA (2013) The impact of secondary compounds and functional characteristics on lichen palatability and decomposition. J Ecol 101:689–700
Article CAS Google Scholar
Asplund J, Gauslaa Y, Merinero S (2016) The role of fungal parasites in tri-trophic interactions involving lichens and lichen-feeding snails. New Phytol 211(4):1352–1357. https://doi.org/10.1111/nph.13975
Article CAS Google Scholar
Asplund J, Gauslaa Y, Merinero S (2018) Low synthesis of secondary compounds in the lichen Lobaria pulmonaria infected by the lichenicolous fungus Plectocarpon lichenum. New Phytol 217(4):1397–1400. https://doi.org/10.1111/nph.14978
Article Google Scholar
Bailey RH (1976) Ecological aspects of dispersal and establishment in lichens. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic, London, pp 215–247
Google Scholar
Bailey RH, James PW (1979) Birds and the dispersal of lichen propagules. Lichenologist 11(1):105–106. https://doi.org/10.1017/S0024282979000141
Article Google Scholar
Barbosa-Silva A, Vasconcellos A (2019) Consumption rate of lichens by Constrictotermes cyphergaster (Isoptera): Effects of C, N, and P contents and ratios. Insects 10(1):23. https://doi.org/10.3390/insects10010023
Article Google Scholar
Barbosa-Silva AM, Alves Santos L, Cáceres M, Vasconcellos A (2019a) Constrictotermes cyphergaster (Blattaria, Termitidae) termite nests as substrates for lichen fixation in the semiarid region of northeastern Brazil. Braz J Biol Rev Bras Biol 80(3):3. https://doi.org/10.1590/1519-6984.222440
Article Google Scholar
Barbosa-Silva AM, da Silva AC, Pereira ECG et al (2019b) Richness of Lichens Consumed by Constrictotermes cyphergaster in the Semi-arid Region of Brazil. Sociobiology 66(1):154. https://doi.org/10.13102/sociobiology.v66i1.3665
Article Google Scholar
Barthlott W (1995) Mimikry: Nachahmung und Täuschung im Pflanzenreich. Biologie in unserer Zeit 25:74–82. https://doi.org/10.1002/biuz.19950250203
Article Google Scholar
Bates ST, Cropsey GWG, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77(4):1309–1314. https://doi.org/10.1128/AEM.02257-10
Article CAS Google Scholar
Baur B, Fröberg L, Baur A (1995) Species diversity and grazing damage in a calcicolous lichen community on top of stone walls in Öland, Sweden. Ann Bot Fenn 32:312–323. https://www.jstor.org/stable/23726274
Google Scholar
Baur B, Fröberg L, Baur A, Guggenheim R, Haase M (2000) Ultrastructure of snail grazing damage to calcicolous lichens. Nordic J Bot 20:119–128. https://doi.org/10.1111/j.1756-1051.2000.tb00741.x
Article Google Scholar
BeGora MD, Fahselt D (2001) Usnic acid and atranorin concentrations in lichens in relation to bands of UV irradiance. Bryologist 104(1):134–140. https://doi.org/10.1639/0007-2745(2001)104[0134:UAAACI]2.0.CO;2
Article CAS Google Scholar
Bendiksby M, Haugan R, Spribille T, Timdal E (2015) Molecular phylogenetics and taxonomy of the Calvitimela aglaea complex (Tephromelataceae, Lecanorales). Mycologia 107(6):1172–1183. https://doi.org/10.3852/14-062
Article CAS Google Scholar
Benesperi R, Tretiach M (2004) Differential land snail damage to selected species of the lichen genus Peltigera. Biochem Syst Ecol 32(2):127–138. https://doi.org/10.1016/S0305-1978(03)00141-8
Article CAS Google Scholar
Berbee ML, Strullu-Derrien C, Delaux P-M et al (2020) Genomic and fossil windows into the secret lives of the most ancient fungi. Nat Rev Microbiol 18:717–730. https://doi.org/10.1038/s41579-020-0426-8
Article CAS Google Scholar
Berner LT, Massey R, Jantz P, et al. (2020) Summer warming explains widespread but not uniform greening in the Arctic tundra biome. Nat Commun 11(article Nr. 4621):12. doi:https://doi.org/10.1038/s41467-020-18479-5
Bertrand RL, Sorensen JL (2018) A comprehensive catalogue of polyketide synthase gene clusters in lichenizing fungi. J Ind Microbiol Biotechnol 45(12):1067–1081. https://doi.org/10.1007/s10295-018-2080-y
Article CAS Google Scholar
Bertrand RL, Sorensen JL (2019a) Transcriptional heterologous expression of two type III PKS from the lichen Cladonia uncialis. Mycol Prog 18:1437–1447
Article Google Scholar
Bertrand R, Sorensen JL (2019b) Lost in translation: challenges with heterologous expression of lichen polyketide synthases. ChemistrySelect 4(21):6473–6483. https://doi.org/10.1002/slct.201901762
Article CAS Google Scholar
Bertrand R, Abdel Hameed M, Sorensen JL (2018) Lichen biosynthetic gene clusters. Part I. Genome sequencing reveals a rich biosynthetic potential. J Nat Prod 91(4). https://doi.org/10.1021/acs.jnatprod.7b00769
Bhattacharyya S, Deep R, Singh S, Nayak B (2016) Lichen secondary metabolites and its biological activity. Am J Pharm Tech Res 6(6):17
Google Scholar
Bissell H (2014) Nutritional implications of the high-elevation lifestyle of Rhinopithecus bieti. In: Grow NB, Gursky-Doyen S, Krzton A (eds) High Altitude Primates, Dev Primat, vol 44, pp 199–210
Chapter Google Scholar
Bjerke JW, Lerfall K, Elvebakk A (2002) Effects of ultraviolet radiation and PAR on the content of usnic and divaricatic acids in two arctic-alpine lichens. Photochem Photobiol Sci 1(9):678–678. https://doi.org/10.1039/b203399b
Article CAS Google Scholar
Bjerke JW, Elvebakk A, Domínguez E, Dahlback A (2005) Seasonal trends in usnic acid concentrations of Arctic, alpine and Patagonian populations of the lichen Flavocetraria nivalis. Phytochemistry 66(3):337–344. https://doi.org/10.1016/j.phytochem.2004.12.007
Article CAS Google Scholar
Boch S, Prati D, Werth S, Rüetschi J, Fischer M (2011) Lichen endozoochory by snails. PLoS One 6(4):e18770. https://doi.org/10.1371/journal.pone.0018770
Article CAS Google Scholar
Boch S, Fischer M, Prati D (2015) To eat or not to eat—relationship of lichen herbivory by snails with secondary compounds and field frequency of lichens. J Plant Ecol 8(6):642–650. https://doi.org/10.1093/jpe/rtv005
Article Google Scholar
Bonnier G (1886) Recherches experimentales sur la synthèse des lichens dans un milieu privé de germes. CR Acad Sci Paris 103:942
Google Scholar
Bonnier G (1889) Recherches sur la synthèse des lichens. Ann Sc Nat Sér 7 9:1–34
Google Scholar
Borchhardt N, Schiefelbein U, Abarca N et al (2017) Diversity of algae and lichens in biological soil crusts of Ardley and King George islands, Antarctica. Antarct Sci 29(3):1–9. https://doi.org/10.1017/S0954102016000638
Article Google Scholar
Bordenave CD, Muggia L, Chiva S, Leavitt SD, Carrasco P, Barreno E (2021) Chloroplast morphology and pyrenoid ultrastructural analyses reappraise the diversity of the lichen phycobiont genus Trebouxia (Chlorophyta). Algal Res, article Nr. 102561; doi: https://doi.org/10.1016/j.algal.2021.102561
Borgato L, Ertz D, Van Rossum F, Verbeken A (2022) The diversity of lichenized trentepohlioid algal (Ulvophyceae) communities is driven by fungal taxonomy and ecological factors. J Phycol 58:582–602. https://doi.org/10.1111/jpy.13252
Article Google Scholar
Boustie J, Grube M (2005) Lichens - A promising source of bioactive secondary metabolites. Plant Genet Resour 3(2):273–287. https://doi.org/10.1079/PGR200572
Article CAS Google Scholar
Boustie J, Tomasi S, Grube M (2011) Bioactive lichen metabolites: alpine habitats as an untapped source. Phytochem Rev 10:287–307. https://doi.org/10.1007/s11101-010-9201-1
Article CAS Google Scholar
Braun H (2011) The Little Lichen Dragon - an extraordinary katydid from the Ecuadorian Andes (Orthoptera, Tettigoniidae, Phaneropterinae, Dysoniini). Zootaxa 3032:33–39. https://doi.org/10.11646/zootaxa.3032.1.3
Article Google Scholar
Brierley WB (1913) The structure and life history of Leptosphaeria lemaneae (Cohn). Mem Manchester Literary Philos Soc 57:1–21
Google Scholar
Brodo IM, Freebury C, Brodo F (2021) A maritime lichen finds a home in Ottawa and it isn’t alone. Trail Landscape 55(4):174–182
Google Scholar
Brunner U, Honegger R (1985) Chemical and ultrastructural studies on the distribution of sporopollenin- like biopolymers in 6 genera of lichen phycobionts. Can J Bot 63(12):2221–2230. https://doi.org/10.1139/b85-315
Article CAS Google Scholar
Bubrick P, Galun M, Frensdorff A (1984) Observations on free-living Trebouxia de Puymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th.Fr. can be found free-living in nature. New Phytol 97:455–462. https://doi.org/10.1111/j.1469-8137.1984.tb03611.x
Article Google Scholar
Büdel B, Henssen A (1988) Trebouxia aggregata und Gloeocapsa sanguinea, Phycobionten in Euopsis granatina (Lichinaceae). Plant Syst Evol 158(2):235–241
Google Scholar
Burr TJ, Caesar A, Schrolh MN (1984) Beneficial plant bacteria. Crit Rev Plant Sci 2(1):1–20. https://doi.org/10.1080/07352688409382186
Article Google Scholar
Buschbom J, Mueller G (2006) Testing “species pair” hypotheses: evolutionary processes in the lichen-forming species complex Porpidia flavocoerulescens and Porpidia melinodes. Mol Biol Evol 23(3):574–586. https://doi.org/10.1093/molbev/msj063
Article CAS Google Scholar
Cadena-Castañeda OJ (2011) La Tribu Dysoniini Parte I: El complejo Dysonia (Orthoptera: Tettigoniidae) y su nueva organización taxonómica. J Orthoptera Res 20(1):51–60. https://doi.org/10.1665/034.020.0105
Article Google Scholar
Cadena-Castañeda OJ (2013) La Tribu Dysoniini Parte III: Adiciones a Los Géneros Apolinaria, Lichenodraculus, Machimoides y Markia (Orthoptera: Tettigoniidae). J Orthoptera Res 22(2):101–123. https://doi.org/10.1665/034.022.0202
Article Google Scholar
Calchera A, Grande FD, Bode HB, Schmitt I (2019) Biosynthetic Gene Content of the ‘Perfume Lichens’ Evernia prunastri and Pseudevernia furfuracea. Molecules 24(203):21. https://doi.org/10.3390/molecules24010203
Article CAS Google Scholar
Cardinale M, Castro JVD, Müller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71. https://doi.org/10.1111/j.1574-6941.2008.00546.x
Article CAS Google Scholar
Casano LM, del Campo EM, García-Breijo FJ et al (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13(3):806–818. https://doi.org/10.1111/j.1462-2920.2010.02386.x
Article CAS Google Scholar
Caseiro C, Dias JNR, Fontes CM, Bule P (2022) From cancer therapy to winemaking: the molecular structure and applications of β-glucans and β-1, 3-glucanases. Int J Molec Sci 23(6, article Nr. 3156); doi: https://doi.org/10.3390/ijms23063156
Cengia Sambo M (1924) Polisymbiosi nei licheni a cianoficee e significao biologico dei cefalodi: Note di biochimica dei licheni. Atti Soc Ital Sci Nat 62:226–238
Google Scholar
Cengia Sambo M (1926) Ancora della polysimbiosi nei licheni ad alghe cianoficee. 1. Batteri simbionti. Atti Soc Ital Sci Nat 64:191–195
Google Scholar
Černajová I, Škaloud P (2019) The first survey of Cystobasidiomycete yeasts in the lichen genus Cladonia; with the description of Lichenozyma pisutiana gen. nov., sp. nov. Fungal Biol 123(9):625–637. https://doi.org/10.1016/j.funbio.2019.05.006
Article Google Scholar
Černajová I, Schiefelbein U, Škaloud P (2022) Lichens from the littoral zone host diverse Ulvophycean photobionts. J Phycol 58(2):267–280. https://doi.org/10.1111/jpy.13234
Article CAS Google Scholar
Cernava T, Berg G, Grube M (2016) High life expectancy of bacteria on lichens. Microb Ecol 72:510–513. https://doi.org/10.1007/s00248-016-0818-5
Article CAS Google Scholar
Cernava T, Aschenbrenner IA, Soh J, Sensen CW, Grube M, Berg G (2018) Plasticity of a holobiont: desiccation induces fasting-like metabolism within the lichen microbiota. ISME J 13(2):10. https://doi.org/10.1038/s41396-018-0286-7
Article CAS Google Scholar
Chakarwarti J, Nayaka S, Srivastava S (2020) Diversity of endolichenic fungi – a review. Asian J Mycol 3(1):490–511. https://doi.org/10.5943/ajom/3/1/18
Article Google Scholar
Chasiri K, McGarry JW, Morand S, Makepeace BL (2015) Symbiosis in an overlooked microcosm: a systematic review of the bacterial flora of mites. Parasitology 142(9):1152–1162. https://doi.org/10.1017/S0031182015000530
Article Google Scholar
Claudel C (2021) The many elusive pollinators in the genus Amorphophallus. Arthropod-Plant Interactions 15:833–844. https://doi.org/10.1007/s11829-021-09865-x. https://www.researchgate.net/publication/354643103_The_many_elusive_pollinators_in_the_genus_Amorphophallus
Article Google Scholar
Claudel C, Lev-Yadun S, Hetterscheid W, Schultz M (2019) Mimicry of lichens and cyanobacteria on tree-sized Amorphophallus petioles results in their masquerade as inedible tree trunks. Bot J Linn Soc 190(2):192–214. https://doi.org/10.1093/botlinnean/boz014
Article Google Scholar
Coca LF, Lücking R, Moncada B (2018) Two new, sympatric and semi-cryptic species of Sulzbacheromyces (Lichenized Basidiomycota, Lepidostromatales) from the Chocó Biogeographic Region in Colombia. Bryologist 121(3):297–305. https://doi.org/10.1639/0007-2745-121.3.297
Article Google Scholar
Cornejo C, Scheidegger C (2013) New morphological aspects of cephalodium formation in the lichen Lobaria pulmonaria (Lecanorales, Ascomycota). Lichenologist 45(6):77–87. https://doi.org/10.1017/S0024282912000631
Article Google Scholar
Cornejo C, Scheidegger C (2016) Cyanobacterial gardens: the liverwort Frullania asagrayana acts as a reservoir of lichen photobionts. Env Microbiol Rep 8(3):352–357. https://doi.org/10.1111/1758-2229.12386
Article CAS Google Scholar
Crawford SD (2019) Lichens used in traditional medicine. In: Ranković B (ed) Lichen secondary metabolites, 2nd edn. Springer Nature Switzerland AG, pp 31–97. https://doi.org/10.1007/978-3-030-16814-8_2
Chapter Google Scholar
Crespo A, Pérez-Ortega S (2009) Cryptic species and species pairs in lichens: A discussion on the relationship between molecular phylogenies and morphological characters. An Jardín Bot Madrid 66(1):71–81. https://doi.org/10.3989/ajbm.2225
Article Google Scholar
Crittenden PD, David JC, Hawksworth DL, Campbell FS (1995) Attempted isolation and success in the culturing of a broad spectrum of lichen-forming and lichenicolous fungi. New Phytol 130(2):267–297
Article Google Scholar
Culberson CF (1969) Chemical and botanical guide to lichen products. University of North Carolina Press, 628 pp
Google Scholar
Culberson CF (1970) Supplement to “chemical and botanical guide to lichen products”. Bryologist 73:177–377
Article CAS Google Scholar
Culberson CF, Armaleo D (1992) Induction of a complete secondary-product pathway in a cultured lichen fungus. Exp Mycol 16(1):52–63. https://doi.org/10.1016/0147-5975(92)90041-O
Article CAS Google Scholar
Culberson CF, Elix JA (1989) Lichen substances. Methods Plant Biochem 1:509–535. https://doi.org/10.1016/B978-0-12-461011-8.50021-4
Article CAS Google Scholar
Culberson CF, Culberson W, Johnson A (1977) Second supplement to “chemical and botanical guide to lichen products”. American Bryological and Lichenologial Society, St. Louis, 400 p
Google Scholar
Dal Grande F, Beck A, Cornejo C et al (2014) Molecular phylogeny and symbiotic selectivity of the green algal genus Dictyochloropsis s.l. (Trebouxiophyceae): a polyphyletic and widespread group forming photobiont-mediated guilds in the lichen family Lobariaceae. New Phytol 202(2):455–470. https://doi.org/10.1111/nph.12678
Article CAS Google Scholar
Dal-Forno M, Kaminsky L, Rosentreter R, McMullin RT, Aptroot A, Lücking R (2019) A first phylogenetic assessment of Dictyonema s.lat. in southeastern North America reveals three new basidiolichens, described in honour of James D. Lawrey. Plant Fungal Syst 64(2):383–392. https://doi.org/10.2478/pfs-2019-0025
Article Google Scholar
Darienko T, Gustavs L, Eggert A, Wolf W, Pröschold T (2015) Evaluating the species boundaries of green microalgae (Coccomyxa, Trebouxiophyceae, Chlorophyta) using integrative taxonomy and DNA barcoding with further implications for the species identification in environmental samples. PLoS One 10(6): e0127838, 31 p; doi: https://doi.org/10.1371/journal.pone.0127838
Davison J (1988) Plant beneficial bacteria. Biotechnology 6:282–286
CAS Google Scholar
de Bary A (1879) Die Erscheinung der Symbiose. Verlag Karl J, Trübner, Strassburg, p 30
Google Scholar
de Carolis R, Cometto A, Moya P, et al. (2022) Photobiont diversity in lichen symbioses from extreme environments. Front Microbiol 13 (article Nr. 809804):21. doi: https://doi.org/10.3389/fmicb.2022.809804
del Cortona A, Jackson CJ, Bucchini F et al (2020) Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds. PNAS 117(5):2551–2559. https://doi.org/10.1073/pnas.1910060117
Article CAS Google Scholar
del Hoyo A, Álvarez R, del Campo EM, Gasulla F, Barreno E, Casano LM (2011) Oxidative stress induces distinct physiological responses in the two Trebouxia phycobionts of the lichen Ramalina farinacea. Ann Bot 107(1):109–118. https://doi.org/10.1093/aob/mcq206
Article CAS Google Scholar
Demoulin CF, Lara YJ, Cornet L et al (2019) Cyanobacteria evolution: insight from the fossil record. Free Radical Bio Med 140:206–223. https://doi.org/10.1016/j.freeradbiomed.2019.05.007
Article CAS Google Scholar
den Herder M, Kytoviita MM, Niemela P (2003) Growth of reindeer lichens and effects of reindeer grazing on ground cover vegetation in a Scots pine forest and a subarctic heathland in Finnish Lapland. Ecography 26(1):3–12. https://doi.org/10.1034/j.1600-0587.2003.03211.x
Article Google Scholar
Díaz EM, Zamora JC, Ruibal C et al (2020) Axenic culture and biosynthesis of secondary compounds in lichen symbiotic fungi, the Parmeliaceae. Symbiosis 82(1–2):1–15. https://doi.org/10.1007/s13199-020-00719-3
Article CAS Google Scholar
Diederich P, Lawrey JD, Ertz D (2018) The 2018 classification and checklist of lichenicolous fungi, with 2000 non-lichenized, obligately lichenicolous taxa. Bryologist 121(3):340–425. https://doi.org/10.1639/0007-2745-121.3.340
Article Google Scholar
Divakar PK, Crespo A, Wedin M et al (2015) Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi. New Phytol 208:1217–1226. https://doi.org/10.1111/nph.13553
Article CAS Google Scholar
Dohi T, Ohmura Y, Yoshimura K et al (2021) Radiocaesium accumulation capacity of epiphytic lichens and adjacent barks collected at the perimeter boundary site of the Fukushima Dai-ichi Nuclear Power Station. PLoS One 16(5):16. https://doi.org/10.1371/journal.pone.0251828
Article CAS Google Scholar
Du Z-Y, Zienkiewicz K, Vande Pol N, Ostrom NE, Benning C, Bonito GM (2019) Algal-fungal symbiosis leads to photosynthetic mycelium. eLife 8:e47815. 22 p. doi:https://doi.org/10.7554/eLife.47815.001
Dughi R (1937) Une cephalodie libre lichenogène: le Dendriscocaulon bolacinum Nyl. Bull Soc Bot France 84:430–437
Article Google Scholar
Edwards D, Axe L (2012) Evidence for a fungal affinity for Nematasketum, a close ally of Prototaxites. Bot J Linn Soc 168(1):1–18. https://doi.org/10.1111/j.1095-8339.2011.01195.x
Article Google Scholar
Edwards D, Selden PA, Richardson JB, Axe L (1995) Coprolites as evidence for plant–animal interaction in Siluro–Devonian terrestrial ecosystems. Nature 377:329–331. https://doi.org/10.1038/377329a0
Article CAS Google Scholar
Edwards D, Axe L, Honegger R (2013) Contributions to the diversity in cryptogamic covers in the mid-Palaeozoic: Nematothallus revisited. Bot J Linn Soc 173(5):505–534. https://doi.org/10.1111/boj.12119
Article Google Scholar
Edwards HGM, Seaward MRD, Preece TF, Jorge-Villar SE, Hawksworth DL (2017) Raman spectroscopic analysis of the effect of the lichenicolous fungus Xanthoriicola physciae on its lichen host. Symbiosis 71(1):57–56. https://doi.org/10.1007/s13199-016-0447-2
Article CAS Google Scholar
Edwards D, Honegger R, Axe L, Morris JL (2018) Anatomically preserved Silurian ‘nematophytes’ from the Welsh Borderland (UK). Bot J Linn Soc 187(2):272–291. https://doi.org/10.1093/botlinnean/boy022
Article Google Scholar
Edwards D, Axe L, Morris JL, Boddy L, Selden PA (2020) Further evidence for fungivory in the Lower Devonian (Lochkovian) of the Welsh Borderland, UK. PalZ 94:603–618. https://doi.org/10.1007/s12542-019-00503-9
Article Google Scholar
Elbert W, Weber B, Burrows S et al (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462. https://doi.org/10.1038/ngeo1486
Article CAS Google Scholar
Elix JA, Stocker-Wörgötter E (2008) Biochemistry and secondary metabolites. In: Nash TH (ed) Lichen biology. Cambridge University Press, Cambridge, pp 104–133. https://doi.org/10.1017/CBO9780511790478.008
Chapter Google Scholar
Elliott JC, Dover SD (1982) X-ray microtomography. J Microsc 126(2):211–213. https://doi.org/10.1111/j.1365-2818.1982.tb00376.x
Article CAS Google Scholar
Englund B (1977) The physiology of the lichen Peltigera aphthosa, with special reference to the blue-green phycobiont (Nostoc sp.). Physiol Plant 41:298–304. https://doi.org/10.1111/j.1399-3054.1977.tb04887.x
Article CAS Google Scholar
Erlacher A, Cernava T, Cardinale M, et al. (2015) Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol 6 (article Nr. 53), 9 p. doi: https://doi.org/10.3389/fmicb.2015.00053
Ertz D, Guzow-Krzemińska B, Thor G, Łubek A, Kukwa M (2018) Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Nat Res 8(1):15. https://doi.org/10.1038/s41598-018-23219-3
Article CAS Google Scholar
Eymann C, Lassek C, Wegner U et al (2017) Symbiotic Interplay of fungi, algae, and bacteria within the lung lichen Lobaria pulmonaria L. Hoffm. as assessed by state-of-the-art metaproteomics. J Proteome Res 16(6):2160–2173. https://doi.org/10.1021/acs.jproteome.6b00974
Article CAS Google Scholar
Fang H, Labandeira CC, Ma Y, et al. (2020) Lichen mimesis in mid-Mesozoic lacewings. eLife 9: e59007. 15 p. doi:https://doi.org/10.7554/eLife.59007
Farkas E, Pocs T (1989) Foliicolous lichen-mimicry of a rainforest treefrog? Acta Bot Hung 35(1-4):73–76
Google Scholar
Fernandez-Marin B, Artetxe U, Becerril JM, Martinez-Abaigar J, Núñez-Olivera E, Garcia Plazaola JI (2018) Can parietin transfer energy radiatively to photosynthetic pigments? Molecules 23(7):1741. https://doi.org/10.3390/molecules23071741
Article CAS Google Scholar
Finger-Higgens R, Duniway MC, Fick S, et al. (2022) Decline in biological soil crust N-fixing lichens linked to increasing summertime temperatures. PNAS 119(16): e2120975119. 8 p. doi:https://doi.org/10.1073/pnas.2120975119
Flechtner V, Pietrasiak N, Lewis LA (2013) Newly revealed diversity of green microalgae from wilderness areas of Joshua Tree National Park (JTNP). Monogr West N. Am Nat 6(1):42–63. https://doi.org/10.2307/23375562
Article Google Scholar
Follmann G (1964) Nebelflechten als Futterpflanzen des Küstenguanacos. Naturwissenschaften 51:19–20
Article Google Scholar
Fraser RH, Lantz TC, Olthof I, Kokelj SV, Sims RA (2014) Warming-Induced shrub expansion and lichen decline in the Western Canadian Arctic. Ecosystems 17(7):1151–1168. https://doi.org/10.1007/s10021-014-9783-3
Article Google Scholar
Friedl T (1987) Thallus development and phycobionts of the parasitic lichen Diploschistes muscorum. Lichenologist 19:183–191. https://doi.org/10.1017/S002428298700015X
Article Google Scholar
Fröberg L, Björn LO, Baur A, Baur B (2001) Viability of lichen photobionts after passing through the digestive tract of a land snail. Lichenologist 33:543–550. https://doi.org/10.1006/lich.2001.0355
Article Google Scholar
Fröberg L, Solhøy T, Baur A, Baur B (2003) Lichen specificity of Oribatid mites (Acari; Oribatida) on limestone walls in the Great Alvar of Öland, Sweden. Entomol Tidskr 124(3):177–182
Google Scholar
Fryday AM, Schmitt I, Pérez-Ortega S (2017) The genus Endocena (Icmadophilaceae): DNA evidence suggests the same fungus forms different morphologies. Lichenologist 49(4):347–363. https://doi.org/10.1017/S0024282917000317
Article Google Scholar
Gadea A, Charrier M, Fanuel M et al (2019) Overcoming deterrent metabolites by gaining essential nutrients: a lichen/snail case study. Phytochemistry 164:86–93. https://doi.org/10.1016/j.phytochem.2019.04.019
Article CAS Google Scholar
Gagunashvili AN, Davíðsson SP, Jónsson ZO, Andrésson ÓS (2009) Cloning and heterologous transcription of a polyketide synthase gene from the lichen Solorina crocea. Mycol Res 113(3):354–363. https://doi.org/10.1016/j.mycres.2008.11.011
Article CAS Google Scholar
Gao H, Zou J, Li J, Zhao H (2016) Endolichenic fungi: a potential treasure trove for discovery of special structures and bioactive compounds. Stud Nat Prod Chem 48:347–397. https://doi.org/10.1016/B978-0-444-63602-7.00011-4
Article CAS Google Scholar
Garbary DJ, London JF (1995) The Ascophyllum/Polysiphonial/Mycosphaerella symbiosis V. Fungal infection protects A. nosodum from desiccation. Bot Mar 38(6):529–533. https://doi.org/10.1515/botm.1995.38.1-6.529
Article Google Scholar
Garcia-Pichel F, Lombard J, Soule T, Dunaj S, Wu SH, Wojciechowsk MF (2019) Timing the evolutionary advent of cyanobacteria and the Later Great Oxidation Event using gene phylogenies of a sunscreen. mBio 10(3): e00561-19. 14 p. doi: https://doi.org/10.1128/mBio.00561-19
Garrido-Benavent I, Pérez-Ortega S (2017) Past, present, and future research in bipolar lichen-forming fungi and their photobionts. Am J Bot 104(11):1660–1674. https://doi.org/10.3732/ajb.1700182
Article Google Scholar
Gasulla F, Barrasa JM, Casano LM, del Campo EM (2020) Symbiont composition of the basidiolichen Lichenomphalia meridionalis varies with altitude in the Iberian Peninsula. Lichenologist 52(1):17–26. https://doi.org/10.1017/S002428291900046X
Article Google Scholar
Gauslaa Y (2005) Lichen palatability depends on investments in herbivore defence. Oecologia 143(1):94–105. https://doi.org/10.1007/s00442-004-1768-z
Article Google Scholar
Gauslaa Y, Holien H, Ohlson M, Solhoy T (2006) Does snail grazing affect growth of the old forest lichen Lobaria pulmonaria? Lichenologist 38:587–593
Article Google Scholar
Gavazov KS, Soudzilovskaia NA, Logtestijn RSPV, Braster M, Cornelissen JHC (2010) Isotopic analysis of cyanobacterial nitrogen fixation associated with subarctic lichen and bryophyte species. Plant Soil 333(1):507–517. https://doi.org/10.1007/s11104-010-0374-6
Article CAS Google Scholar
Gerasimova J, Ruthensteiner B, Beck A (2021) MicroCT as a useful tool for analysing the 3D structure of lichens and quantifying Internal cephalodia in Lobaria pulmonaria. Appl Microbiol 1:189–200. https://doi.org/10.3390/applmicrobiol1020015
Article Google Scholar
Gerasimova J, Beck A, Werth S, Resl P (2022) High diversity of type I polyketide genes in Bacidia rubella as revealed by the comparative analysis of 23 lichen fungal genomes. J Fungi 8(449):25. https://doi.org/10.1101/2022.02.10.479404
Article Google Scholar
Gerson U (1973) Lichen-arthropod associations. Lichenologist 5:434–443
Article Google Scholar
Gerson U, Seaward MRD (1977) Lichen-invertebrate associations. In: Seaward MRD (ed) Lichen ecology. Academic, London, pp 69–119
Google Scholar
Goffinet B, Bayer RJ (1997) Characterization of mycobionts of photomorph pairs in the Peltigerineae (lichenized ascomycetes) based on internal transcribed spacer sequences of the nuclear ribosomal DNA. Fungal Genet Biol 21:228–237. https://doi.org/10.1006/fgbi.1997.0977
Article CAS Google Scholar
González I, Ayuso-Sacido A, Anderson A, Genilloud O (2005) Actinomycetes isolated from lichens: evaluation of their diversity and detection of biosynthetic gene sequences. FEMS Microbiol Ecol 54(3):401–415. https://doi.org/10.1016/j.femsec.2005.05.004
Article CAS Google Scholar
Graves GR, Dal Forno M (2018) Persistence of transported lichen at a hummingbird nest site. Northeast Nat 25:656–666. https://doi.org/10.1656/045.025.0410
Article Google Scholar
Gressitt JL (1966) The Papuan weevil genus Gymnopholus (Leotopiinae) symbiotic with cryptogamic plants, oribatid mites, rotifers and nematodes. Pacif Insects 8(1):221–280
Google Scholar
Gressitt JL (1970) Papuan weevil genus Gymnopholus: second supplement with studies in epizoic symbiois. Pacif Insects 12:753–762
Google Scholar
Gressitt JL (1977) Symbiosis runs wild in a Lilliputian forest growing on the back of high-living weevils in New Guinea. Smithsonian 7(11):135–140
Google Scholar
Gressitt JL, Sedlacek J, Szent-Ivany JJH (1965) Flora and fauna on backs of large Papuan moss-forest weevils. Science 150(3705):1833–1835. https://doi.org/10.1126/science.150.3705.1833
Article CAS Google Scholar
Grimm M, Grube M, Schiefelbein U, Zühlke D, Bernhardt J, Riedel K (2021) The lichens’ microbiota, still a mystery? Front Microbiol 12(Article 623839):101–125; doi: https://doi.org/10.3389/fmicb.2021.623839
Grube M, Berg G (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23(3):72–85. https://doi.org/10.1016/j.fbr.2009.10.001
Article Google Scholar
Grube M, Cardinale M, Berg G (2012) Bacteria and lichen symbiosis. In: Hock B (ed) Fungal associations. The Mycota IX, 2nd edn. Springer, Berlin, pp 363–372
Chapter Google Scholar
Grube M, Aschenbrenner IA, Cernava T, Berg G (2016) Lichen–bacterial interactions. In: Kubicek CP, Druzhinina IS (eds) The mycota IV environmental and microbial relationships. Springer, pp 179–188. https://doi.org/10.1007/978-3-319-29532-9_9
Chapter Google Scholar
Grueter CC, Li D, Ren B, Wei F, van Schaik CP (2009) Dietary profile of Rhinopithecus bieti and its socioecological implications. Int J Primatol 30(4):601–624. https://doi.org/10.1007/s10764-009-9363-0
Article Google Scholar
Grueter CC, Li D, Ren B, Xiang Z, Li M (2012) Food abundance is the main determinant of high-altitude range use in snub-nosed monkeys. Int J Zool 2012(Article ID 739419):4. doi:https://doi.org/10.1155/2012/739419
Hafellner J, Calatayud V (1999) Lichenostigma cosmopolites, a common lichenicolous fungus on Xanthoparmelia species. Mycotaxon 72:107–114. https://doi.org/10.4039/tce.2012.93
Article Google Scholar
Hansell MH (1996) The function of lichen flakes and white spider cocoons on the outer surface of birds’ nests. J Nat Hist 30:303–311. https://doi.org/10.1080/00222939600771181
Article Google Scholar
Hartl C, Schmidt AR, Heinrichs J et al (2015) Lichen preservation in amber: morphology, ultrastructure, chemofossils, and taphonomic alteration. Foss Rec 18:127–135. https://doi.org/10.5194/fr-18-127-2015
Article Google Scholar
Hawksworth DL (2000) Freshwater and marine lichen-forming fungi. In: Hyde KD, Ho WH, Pointing SB (eds) Aquatic mycology across the millennium. Fungal Divers 5:1–7
Google Scholar
Hawksworth DL (2012) Stratified algal and cyanobacterial lichens from the Lower Devonian. IMA Fungus 3(2):56–57. http://www.imafungus.org/Issue/32/06.pdf
Article Google Scholar
Hawksworth DL (2015) Lichenization: the origins of a fungal life-style. In: Upreti DK et al (eds) Recent advances in lichenology, Springer, pp 1–10. https://doi.org/10.1007/978-81-322-2235-4_1
Hawksworth DL (2016) Transcriptomics leads to discovery of basidiomycete yeasts on lichen cortices – and speculation as to function. IMA Fungus 7:A65–A68. https://springerlink.bibliotecabuap.elogim.com/article/10.1007/BF03449421
Article Google Scholar
Hawksworth DL, Grube M (2020) Lichens redefined as complex ecosystems. New Phytol 227:1281–1283. https://doi.org/10.1111/nph.16630
Article Google Scholar
Hawksworth DL, Honegger R (1994) The lichen thallus: symbiotic phenotype and its responses to gall producers. In: Williams MC (ed) Plant galls: organisms, interactions. Clarendon Press, Oxford, pp 77–98
Google Scholar
Hayward GD, Rosentreter R (1994) Lichens as nesting material for northern flying squirrels in the Northern Rocky Mountains. J Mammal 75:663–673. https://doi.org/10.2307/1382514
Article Google Scholar
Heggberget TM, Gaare E, Ball JP (2002) Reindeer (Rangifer tarandus) and climate change: importance of winter forage. Rangifer 22(1):13–32. https://doi.org/10.7557/2.22.1.388
Article Google Scholar
Heggenes J, Odland A, Chevalier T et al (2017) Herbivore grazing—or trampling? Trampling effects by a large ungulate in cold high- latitude ecosystems. Eco Evol 7:6423–6431. https://doi.org/10.1002/ece3.3130
Article Google Scholar
Heggenes J, Fagertun C, Odland A, Bjerketvedt DK (2020) Soft resilience: moisture-dependent lichen elasticity buffer herbivore trampling in cold alpine-tundra ecosystems. Polar Biol 43:789–799. https://doi.org/10.1007/s00300-020-02685-4
Article Google Scholar
Hei Y, Zhang H, Tan N, Zhou Y, Wei X (2021) Antimicrobial activity and biosynthetic potential of cultivable actinomycetes associated with Lichen symbiosis from Qinghai-Tibet Plateau. Microbiol Res 244(article Nr. 126652):14. https://doi.org/10.1016/j.micres.2020.126652
Article CAS Google Scholar
Hejnowicz Z, Barthlott W (2005) Structural and mechanical peculiarities of the petioles of giant leaves of Amorphophallus (Araceae). Am J Bot 92:391–403. https://doi.org/10.3732/ajb.92.3.391
Article Google Scholar
Henderson A, Hackett DJ (1986) Lichen and algal camouflage and dispersal in the psocid nymph Trichadenotecnum fasciatum. Lichenologist 18(2):199–200
Article Google Scholar
Hendrickson JR, Weber WA (1964) Lichens on Galapagos Giant Tortoises. Science 144(3625):1463. https://doi.org/10.1126/science.144.3625.1463
Article CAS Google Scholar
Henskens FL, Green AT, Wilkins A (2012) Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis. Ann Bot 110(3):555–563. https://doi.org/10.1093/aob/mcs108
Article CAS Google Scholar
Hertel H, Rambold G (1988) Cephalodiate Arten der Gattung Lecidea sensu lato (Ascomycetes lichenisati). Plant Syst Evol 158:289–312
Article Google Scholar
Hesbacher S, Baur B, Baur A, Proksch P (1995) Sequestration of lichen compounds by three species of terrestrial snails. J Chem Ecol 21:233–246
Article CAS Google Scholar
Hill DJ (1976) The physiology of lichen symbiosis. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic, London, pp 457–496. (+ 1 plate)
Google Scholar
Hill DJ (1992) An overlooked symbiosis. Photosynth Res 34:339–340. https://docksci.com/an-overlooked-symbiosis_5bb1ecf9d64ab20aa14f5a33.html
Article CAS Google Scholar
Hodkinson BP, Lendemer J (2013) Next-generation sequencing reveals sterile crustose lichen phylogeny. Mycosphere 4(6):1028–1039. https://doi.org/10.5943/mycosphere/4/6/1
Article Google Scholar
Hodkinson BP, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49(3):163–180. https://doi.org/10.1007/s13199-009-0049-3
Article CAS Google Scholar
Hodkinson BP, Moncada B, Lücking R (2014) Lepidostromatales, a new order of lichenized fungi (Basidiomycota, Agaricomycetes), with two new genera, Ertzia and Sulzbacheromyces, and one new species, Lepidostroma winklerianum. Fungal Divers 64(1):165–179. https://doi.org/10.1007/s13225-013-0267-0
Article Google Scholar
Hoffman Y, Aflalo C, Zarka A, Gutman J, James TY, Boussiba S (2008) Isolation and characterization of a novel chytrid species (phylum Blastocladiomycota), parasitic on the green alga Haematococcus. Mycol Res 112(1):70–81. https://doi.org/10.1016/j.mycres.2007.09.002
Article CAS Google Scholar
Högnabba F (2006) Molecular phylogeny of the genus Stereocaulon (Stereocaulaceae, lichenized ascomycetes). Mycol Res 110(9):1080–1092. https://doi.org/10.1016/j.mycres.2006.04.013
Article CAS Google Scholar
Holyoak GA, Holyoak D, Yanes Y, Alonso MR, Ibáñez M (2011) Two new Napaeus species from La Gomera and La Palma (Canary Islands) (Gastropoda: Pulmonata: Enidae). Arch Molluskenkd 140(1):37–48. https://doi.org/10.1127/arch.moll/1869-0963/140/037-048
Article Google Scholar
Hom EFY, Murray AW (2014) Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345(6192):94–98. https://doi.org/10.1126/science.1253320
Article CAS Google Scholar
Honegger R (1985) Ascus structure and ascospore formation in the lichen-forming Chaenotheca chrysocephala (Caliciales). Sydowia Ser II 38:146–157
Google Scholar
Honegger R (1986a) Ultrastructural studies in lichens. I. Haustorial types and their frequencies in a range of lichens with trebouxioid phycobionts. New Phytol 103(4):785–795. https://doi.org/10.1111/j.1469-8137.1986.tb00853.x
Article Google Scholar
Honegger R (1986b) Ultrastructural studies in lichens. II. Mycobiont and photobiont cell wall surface layers and adhering crystalline lichen products in four Parmeliaceae. New Phytol 103:797–808. https://doi.org/10.1111/J.1469-8137.1986.TB00854.X
Article CAS Google Scholar
Honegger R (1991a) Functional aspects of the lichen symbiosis. Annu Rev Plant Physiol Plant Mol Biol 42:553–578. https://doi.org/10.1146/annurev.pp.42.060191.003005
Article CAS Google Scholar
Honegger R (1991b) Symbiosis and fungal evolution: symbiosis and morphogenesis. In: Margulis L, Fester R (eds) Evolution and Speciation: symbiosis as a source of evolutionary innovation. MIT Press, Cambridge, MA, pp 319–340
Google Scholar
Honegger R (1993) Developmental biology of lichens. New Phytol 125(4):659–677. https://doi.org/10.1111/j.1469-8137.1993.tb03916.x
Article Google Scholar
Honegger R (1997) Metabolic interactions at the mycobiont-photobiont interface in lichens. In: Carroll GC, Tudzynski P (eds) The Mycota plant relationships, The Mycota, vol V, 1st edn. Springer, Berlin, pp 209–221
Chapter Google Scholar
Honegger R (2000) Great discoveries in bryology and lichenology - Simon Schwendener (1829-1919) and the dual hypothesis of lichens. Bryologist 103(2):307–313. https://doi.org/10.1639/0007-2745(2000)103[0307:SSATDH]2.0.CO;2
Article Google Scholar
Honegger R (2003) The impact of different long-term storage conditions on the viability of lichen-forming ascomycetes and their green algal photobiont, Trebouxia spp. Plant Biol 5(3):324–330. https://doi.org/10.1055/s-2003-40794
Article Google Scholar
Honegger R (2009) Lichen-forming fungi and their photobionts. In: Deising H (ed) The Mycota Plant relationships. The Mycota, vol V, 2nd edn. Springer, Berlin, pp 305–333
Google Scholar
Honegger R (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts. In: Hock B (ed) Fungal associations. The Mycota IX, 2nd edn. Springer, Berlin, pp 287–339
Chapter Google Scholar
Honegger R (2018) Fossil lichens from the Lower Devonian and their bacterial and fungal epi- and endobionts. In: Blanz P (ed) Biodiversity and ecology of fungi, Lichens, and Mosses Kerner von Marilaun Workshop 2015 in memory of Josef Poelt, Biosystematics and ecology series, vol 34. Verlag der Österreichischen Akademie der Wissenschaften, Wien, pp 547–563
Google Scholar
Honegger R, Bartnicki-Garcia S (1991) Cell wall structure and composition of cultured mycobionts from the lichens Cladonia macrophylla, Cladonia caespiticia, and Physcia stellaris (Lecanorales, Ascomycetes). Mycol Res 95:905–914
Article CAS Google Scholar
Honegger R, Brunner U (1981) Sporopollenin in the cell wall of Coccomyxa and Myrmecia phycobionts of various lichens: an ultrastructural and chemical investigation. Can J Bot 59:2713–2734. https://doi.org/10.1139/b81-322
Article CAS Google Scholar
Honegger R, Haisch A (2001) Immunocytochemical location of the (1→3) (1→4)-β-glucan lichenin in the lichen-forming ascomycete Cetraria islandica (Icelandic moss). New Phytol 150:739–746. https://doi.org/10.1046/j.1469-8137.2001.00122.x
Article CAS Google Scholar
Honegger R, Hugelshofer G (2000) Water relations in the Peltigera aphthosa group visualized with LTSEM techniques. In: B. Schroeter, T.G.A. Green (ed) New aspects in cryptogamic research contributions in honour of Ludger Kappen. Bibl Lichenol 75, J Cramer: 113–126
Google Scholar
Honegger R, Kutasi V (1990) Anthraquinone production in three aposymbiotically cultured teloschistalean lichen mycobionts: the role of the carbon source. In: Nardon P, Gianinazzi-Pearson V, Grenier AM, Margulis L, Smith DC (eds) Endocytobiology IV. INRA, Paris, pp 175–178
Google Scholar
Honegger R, Peter M (1994) Routes of solute translocation and the location of water in heteromerous lichens visualized with cryotechniques in light and electron microscopy. Symbiosis 16(2):167–186
Google Scholar
Honegger R, Zippler U (2007) Mating systems in representatives of Parmeliaceae, Ramalinaceae and Physciaceae (Lecanoromycetes, lichen-forming ascomycetes). Mycol Res 111:424–432. https://doi.org/10.1016/j.mycres.2007.02.005
Article CAS Google Scholar
Honegger R, Peter M, Scherrer S (1996) Drought-induced structural alterations at the mycobiont-photobiont interface in a range of foliose macrolichens. Protoplasma 190(3):221–232. https://doi.org/10.1007/BF01281320
Article Google Scholar
Honegger R, Zippler U, Gansner H, Scherrer S (2004a) Mating systems in the genus Xanthoria (lichen-forming ascomycetes). Mycol Res 108:480–488. https://doi.org/10.1017/S0953756204009682
Article CAS Google Scholar
Honegger R, Zippler U, Scherrer S, Dyer P (2004b) Genetic diversity in Xanthoria parietina (L.) Th. Fr. (lichen-forming ascomycete) from worldwide locations. Lichenologist 36(6):381–390. https://doi.org/10.1017/S002428290401477X
Article Google Scholar
Honegger R, Edwards D, Axe L (2013a) The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytol 197(1):264–275. https://doi.org/10.1111/nph.12009
Article Google Scholar
Honegger R, Axe L, Edwards D (2013b) Bacterial epibionts and endolichenic actinobacteria and fungi in the Lower Devonian lichen Chlorolichenomycites salopensis. Fungal Biol 117(7–8):512–518. https://doi.org/10.1016/j.funbio.2013.05.003
Article CAS Google Scholar
Honegger R, Edwards D, Axe L, Strullu-Derrien C (2018) Fertile Prototaxites taiti: a basal ascomycete with inoperculate, polysporous asci lacking croziers. Philos Trans R Soc Lond B 373(1739. 20170146):14. doi: https://doi.org/10.1098/rstb.2017.0146
Hounslow MW (2020) Chronostratigraphy reference module in earth systems and environmental sciences; Encyclopedia of Geology, 2e; doi: https://doi.org/10.1016/B978-0-08-102908-4.00060-6
Huiskes AH, Gremmen NJ, Bergstrom DM et al (2014) Aliens in Antarctica: assessing transfer of plant propagules by human visitors to reduce invasion risk. Biol Conserv 171:278–284. https://doi.org/10.1016/j.biocon.2014.01.038
Article Google Scholar
Huneck S (2001) New results on the chemistry of lichen substances. Fortschritte der Chemie organischer Naturstoffe/Progress in the chemistry of organic natural products 81:1–276
CAS Google Scholar
Huneck S, Yoshimura I (1996) Identification of Lichen substances. Springer, Berlin, p 508
Book Google Scholar
Hunter L, Dewanckele J (2021) Evolution of micro-CT: moving from 3D to 4D. Microscopy Today 29(3):28–34. https://doi.org/10.1017/S1551929521000651
Article CAS Google Scholar
Hyvärinen M, Hardling R, Tuomi J (2002) Cyanobacterial lichen symbiosis: the fungal partner as an optimal harvester. Oikos 98(3):498–504. https://doi.org/10.1034/j.1600-0706.2002.980314.x
Article Google Scholar
Inga B (2007) Reindeer (Rangifer tarandus tarandus) feeding on lichens and mushrooms: traditional ecological knowledge among reindeer-herding Sami in northern Sweden. Rangifer 27(2):93–106. https://doi.org/10.7557/2.27.2.163
Article Google Scholar
Ingelfinger R, Henke M, Roser L, et al. (2020) Unraveling the pharmacological potential of lichen extracts in the context of cancer and inflammation with a broad screening approach. Front Pharmacol 11(article Nr. 1322):14. doi:https://doi.org/10.3389/fphar.2020.01322
Itten B, Honegger R (2010) Population genetics in the homothallic lichen-forming ascomycete Xanthoria parietina. Lichenologist 42(6):751–761. https://doi.org/10.1017/S0024282910000411
Article Google Scholar
Jahns HM (1987) New trends in developmental morphology of the thallus. Bibl Lichenol 25:17–33
Google Scholar
Jahren AH, Porter S, Kuglitsch JJ (2003) Lichen metabolism identified in Early Devonian terrestrial organisms. Geology 31(2):99–102. https://doi.org/10.1130/0091-7613(2003)031<0099:LMIIED>2.0.CO;2
Article CAS Google Scholar
James PW, Henssen A (1976) The morphological and taxonomic significance of cephalodia. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic, London, pp 27–77
Google Scholar
Jeong M-H, Park C-h, Kim JA, et al. (2021) Production and activity of cristazarin in the lichen-forming fungus Cladonia metacorallifera. J Fungi 7(8, article Nr. 601):14. doi: https://doi.org/10.3390/jof7080601
Johansson N, Kaasalainen U, Rikkinen J (2021) Woodpeckers can act as dispersal vectors for fungi, plants, and microorganisms. Ecol Evol 11(12):7154–7163. https://doi.org/10.1002/ece3.7648
Article Google Scholar
Jørgensen PM, Jahns HM (1987) Muhria, a remarkable new lichen genus from Scandinavia. Notes RBG Edinb 44(3):581–599
Google Scholar
Jurina AL, Krassilov VA (2002) Lichenlike fossils from the Givetian of central Kazakhstan. Paleontol Zh 5:100–105
Google Scholar
Kaasalainen U, Heinrichs J, Krings M, et al. (2015) Alectorioid morphologies in paleogene lichens: new evidence and re-evaluation of the fossil Alectoria succini Mägdefrau. PLoS One 10(6, e0129526):12. doi:https://doi.org/10.1371/journal.pone.0129526
Kaasalainen U, Schmidt AR, Rikkinen J (2017) Diversity and ecological adaptations in Palaeogene lichens. Nat Plants 3(5):17049. https://doi.org/10.1038/nplants.2017.49
Article Google Scholar
Kaasalainen U, Kukwa M, Rikkinen J, Schmidt AR (2019) Crustose lichens with lichenicolous fungi from Paleogene amber. Sci Rep-UK 9 (Article Nr. 10360):7. doi:https://doi.org/10.1038/s41598-019-46692-w
Kaasalainen U, Rikkinen J, Schmidt AR (2020) Fossil Usnea and similar fruticose lichens from Palaeogene amber. Lichenologist 52:319–324. https://doi.org/10.1017/S0024282920000286
Article Google Scholar
Karatygin IV, Snigirevskaya NS, Vikulin SV (2009) The most ancient terrestrial lichen Winfrenatia reticulata: a new find and new interpretation. Paleontol J 43:107–114. https://doi.org/10.1134/S0031030109010110
Article Google Scholar
Kealey JT, Craig JP, Barr PJ (2021) Identification of a lichen depside polyketide synthase gene by heterologous expression in Saccharomyces cerevisiae. Metab Eng Commun 13(e00172):6. https://doi.org/10.1016/j.mec.2021.e00172
Article CAS Google Scholar
Kellogg JJ, Raja HA (2017) Endolichenic fungi: a new source of rich bioactive secondary metabolites on the horizon. Phytochem Rev 16:271–293. https://doi.org/10.1007/s11101-016-9473-1
Article CAS Google Scholar
Kettunen E, Schmidt AR, Diederich P, Grabenhorst H, Rikkinen J (2016) Lichen-associated fungi from Paleogene amber. New Phytol 209(3):896–898. https://doi.org/10.1111/nph.13653
Article Google Scholar
Kettunen E, Schmidt AR, Diederich P, Grabenhorst H, Rikkinen J (2018) Diversity of lichen-associated filamentous fungi preserved in European Paleogene amber. Trans R Soc Edinb Earth 107(2–3):311–320. https://doi.org/10.1017/S1755691017000111
Article Google Scholar
Khadhri A, Mendili M, Araújo MEM, Seaward MRD (2019) Comparative study of secondary metabolites and bioactive properties of the lichen Cladonia foliacea with and without the lichenicolous fungus Heterocephalacria bachmannii. Symbiosis 79:25–31. https://doi.org/10.1007/s13199-019-00630-6
Article CAS Google Scholar
Kim JI, Nam SW, So JE, Hong SG, Choi H-G, Shin W (2017) Asterochloris sejongensis sp. nov. (Trebouxiophyceae, Chlorophyta) from King George Island, Antarctica. Phytotaxa 295(1):60–70. https://doi.org/10.11646/phytotaxa.295.1.5
Article Google Scholar
Kirkpatrick RC, Grueter CC (2010) Snub-nosed monkeys: multilevel societies across varied environments. Evol Anthropol 19(3):98–113. https://doi.org/10.1002/evan.20259
Article Google Scholar
König CC, Scherlach K, Schroeckh V et al (2013) Bacterium induces cryptic meroterpenoid pathway in the pathogenic fungus Aspergillus fumigatus. Chembiochem 14(8):938–942. https://doi.org/10.1002/cbic.201300070
Article CAS Google Scholar
Kono M, Kon Y, Ohmura Y, Satta Y, Terai Y (2020) In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in Usnea hakonensis. BMC Genomics 21(671):16. https://doi.org/10.1186/s12864-020-07086-9
Article CAS Google Scholar
Kosecka M, Guzow-Krzemińska B, Černajová I, Skaloud P, Jabłońska A, Kukwa M (2021) New lineages of photobionts in Bolivian lichens expand our knowledge on habitat preferences and distribution of Asterochloris algae. Sci Rep 11(1):13. https://doi.org/10.1038/s41598-021-88110-0
Article CAS Google Scholar
Kosecka M, Kukwa M, Jabłońska A, et al. (2022) Phylogeny and ecology of Trebouxia photobionts from Bolivian lichens. Front Microbiol 13(article Nr. 779784): doi: https://doi.org/10.3389/fmicb.2022.779784
Kotta-Loizou I, Castón JR, Coutts RHA et al (2020) ICTV virus taxonomy profile: Chrysoviridae. J Gen Virol 101(2):143–144. https://doi.org/10.1099/jgv.0.001383
Article CAS Google Scholar
Krespach M, Altares MG, Flak M et al (2020) Lichen-like association of Chlamydomonas reinhardtii and Aspergillus nidulans protects algal cells from bacteria. ISME J 14:2794–2805. https://doi.org/10.1038/s41396-020-0731-2
Article CAS Google Scholar
Kroken S, Taylor JW (2001) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia. Mycologia 93(1):38–53. https://doi.org/10.1080/00275514.2001.12061278
Article CAS Google Scholar
Kukwa M, Pérez-Ortega S (2010) A second species of Botryolepraria from the Neotropics and the phylogenetic placement of the genus within Ascomycota. Mycol Progr 9(3):345–351. https://doi.org/10.1007/s11557-009-0642-0
Article Google Scholar
Lange de la Camp M (1933) Kulturversuche mit Flechtenpilzen (Xanthoria parietina). Arch Mikrobiol 4:379–393
Article Google Scholar
Lange OL, Tenhunen JD (1981) Moisture content and CO₂ exchange of lichens. II. Depression of net photosynthesis in Ramalina maciformis at high water content is caused by increased thallus carbon dioxide diffusion resistance. Oecologia 51(3):426–429. https://doi.org/10.1007/BF00540917
Article CAS Google Scholar
Larsen J, Raisen CL, Ba X et al (2022) Emergence of methicillin resistance predates the clinical use of antibiotics. Nature 602(7895):29. https://doi.org/10.1038/s41586-021-04265-w
Article CAS Google Scholar
Lawrey JD (1980) Calcium accumulation by lichens and transfer to lichen herbivores. Mycologia 72(3):586–594. https://doi.org/10.1080/00275514.1980.12021221
Article Google Scholar
Lawrey JD, Torzilli AP, Chandhoke V (1999) Destruction of lichen chemical defenses by a fungal pathogen. Am J Bot 86(2):184–189
Article CAS Google Scholar
Le Pogam P, Legouin B, Geairon A et al (2016) Spatial mapping of lichen specialized metabolites using LDI-MSI: chemical ecology issues for Ophioparma ventosa. Sci Rep 6(1):9. https://doi.org/10.1038/srep37807
Article CAS Google Scholar
Leavitt SD, Westberg M, Nelsen MP, et al. (2018) Multiple, distinct intercontinental lineages but isolation of Australian populations in a cosmopolitan lichen-forming fungal taxon, Psora decipiens (Psoraceae, Ascomycota). Front Microbiol 9(Article 283):15. doi:https://doi.org/10.3389/fmicb.2018.00283
Leite FSF, Pezzuti TL, de Anchietta Garcia PC (2012) A new species of the Bokermannohyla pseudopseudis group from the Espinhaço Range, Central Bahia, Brazil (Anura: Hylidae). Herpetologica 68(3):401–409. https://doi.org/10.2307/23255791
Article Google Scholar
Lendemer JC, Hodkinson BP (2013) A radical shift in the taxonomy of Lepraria s.l.: molecular and morphological studies shed new light on the evolution of asexuality and lichen growth form diversification. Mycologia 105(4):994–1018. https://doi.org/10.3852/12-338
Article Google Scholar
Lendemer J, Keepers K, Tripp EA, Pogoda CS, Mccain CM, Kane NC (2019) A taxonomically broad metagenomic survey of 339 species spanning 57 families suggests cystobasidiomycete yeasts are not ubiquitous across all lichens. Am J Bot 106(8):1–6. https://doi.org/10.1002/ajb2.1339
Article CAS Google Scholar
Lerch M, Nadyeina O, Scheidegger C (2018) Genetic structure of Lobaria pulmonaria in the Alps as a result of post-glacial recolonization history. Herz 31(1):650–665. https://doi.org/10.13158/heia.31.1.2018.650
Article Google Scholar
Li X-Y, Ang S-J (2009) Winter food habits of the Yunnan Snub-nosed Monkey (Rhinopithecus bieti) found at Mt. Longma, Yunnan. Acta Anthropol Sinica 28(4):391–400
Google Scholar
Lindgren H, Diederich P, Goward T, Myllys L (2015) The phylogenetic analysis of fungi associated with lichenized ascomycete genus Bryoria reveals new lineages in the Tremellales including a new species Tremella huuskonenii hyperparasitic on Phacopsis huuskonenii. Fungal Biol 119(9):844–856. https://doi.org/10.1016/j.funbio.2015.06.005
Article Google Scholar
Liu Y, Li X, Jia R-L, Huang L, Zhou Y, Gao Y (2011) Effects of biological soil crusts on soil nematode communities following dune stabilization in the Tengger Desert, Northern China. Appl Soil Ecol 49(1):118–124. https://doi.org/10.1016/j.apsoil.2011.06.007
Article Google Scholar
Liu X, Stanford CB, Yang J, Yao H, Li Y (2013) Foods eaten by the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China, in relation to nutritional chemistry. Am J Primatol 75(8):860–871. https://doi.org/10.1002/ajp.22149
Article CAS Google Scholar
Liu D, Oh S-O, Park J-S, Hur J-S (2018) New species and new record of genus Chrysothrix (Chrysotrichaceae, Arthoniales) from South Korea and Chile. Mycobiology 46(3):185–191. https://doi.org/10.1080/12298093.2018.1509511
Article Google Scholar
Longcore JE, Qin S, Simmons DR, James TY (2020) Quaeritorhiza haematococci is a new species of parasitic chytrid of the commercially grown alga, Haematococcus pluvialis. Mycologia 112(3):606–615. https://doi.org/10.1080/00275514.2020.1730136
Article CAS Google Scholar
Lopandic K, Molnár O, Prillinger H (2005) Fellomyces mexicanus sp. nov., a new member of the yeast genus Fellomyces isolated from lichen Cryptothecia rubrocincta collected in Mexico. Microbiol Res 160(1):1–11. https://doi.org/10.1016/j.micres.2004.09.004
Article CAS Google Scholar
Lücking R, Bernecker-Lücking A (2000) Lichen feeders and lichenicolous fungi: Do they affect dispersal and diversity in tropical foliicolous lichen communities? Ecotropica 6(1):23–41
Google Scholar
Lücking R, Cáceres M (2002) Foliicolous lichens of the World. Part 1: Genera and selected species I (Introduction) Environmental and Conservation Programs, The Field Museum, Chicago, pp 1–6
Google Scholar
Lücking R, Sipman HJM, Umaña L (2004) TICOLICHEN - The Costa Rican lichen biodiversity inventory as a model for lichen inventories in the tropics. In: Randlane T, Saag A (eds) Lichens in focus. Tartu University Press, Tartu, p 32
Google Scholar
Lücking R, Lumbsch HT, di Stéfano JF et al (2008) Eremithallus costaricensis (Ascomycota: Lichinomycetes: Eremothallales), a new fungal lineage with a novel lichen symbiotic lifestyle discovered in an urban relict forest in Costa Rica. Symbiosis 46(3):161–170
Google Scholar
Lücking R, Mata-Lorenzen J, Dauphin LG (2010) Epizoic liverworts, lichens and fungi growing on Costa Rican Shield Mantis (Mantodea: Choeradodis). Stud Neotrop Fauna E 45:175–186. https://doi.org/10.1080/01650521.2010.532387
Article Google Scholar
Lücking R, Dal-Forno M, Sikaroodi M et al (2014) A single macrolichen constitutes hundreds of unrecognized species. PNAS 111(30):11091–11096. https://doi.org/10.1073/pnas.1403517111
Article CAS Google Scholar
Lücking R, Dal-Forno M, Moncada B et al (2016) Turbo-taxonomy to assemble a megadiverse lichen genus: seventy new species of Cora (Basidiomycota: Agaricales: Hygrophoraceae), honouring David Leslie Hawksworth’s seventieth birthday. Fungal Divers 84(1):1–69. https://doi.org/10.1007/s13225-016-0374-9
Article Google Scholar
Lücking R, Hodkinson BP, Leavitt SD (2017a) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – approaching one thousand genera. Bryologist 119(4):361–416. https://doi.org/10.1639/0007-2745-119.4.361
Article Google Scholar
Lücking R, Moncada B, McCune B et al (2017b) Pseudocyphellaria crocata (Ascomycota: Lobariaceae) in the Americas is revealed to be thirteen species, and none of them is P. crocata. Bryologist 120(4):441–500. https://doi.org/10.1639/0007-2745-120.4.14
Article Google Scholar
Lücking R, Leavitt SD, Hawksworth DL (2021) Species in lichen-forming fungi: balancing between conceptual and practical considerations, and between phenotype and phylogenomics. Fungal Divers 109:99–154. https://doi.org/10.1007/s13225-021-00477-7
Article Google Scholar
Lücking R, Dal-Forno M, Lawrey JD et al (2022) Ten new species of lichenized Basidiomycota in the genera Dictyonema and Cora (Agaricales: Hygrophoraceae), with a key to all accepted genera and species in the Dictyonema clade. Phytotaxa 139(1):1–38. https://doi.org/10.11646/phytotaxa.139.1.1
Article Google Scholar
Lutzoni F, Nowak MD, Alfaro ME et al (2018) Contemporaneous radiations of fungi and plants linked to symbiosis. Nat Commun 9(1):11. https://doi.org/10.1038/s41467-018-07849-9
Article CAS Google Scholar
Macedo DCS, Almeida FJF, Wanderley MSO et al (2021) Usnic acid: from an ancient lichen derivative to promising biological and nanotechnology applications. Phytochem Rev 20(4):609–830. https://doi.org/10.1007/s11101-020-09717-1
Article CAS Google Scholar
MacGinitie H (1937) The flora of the Weaverville beds of Trinity County, California, with descriptions of the plant-bearing beds. In: Sanborn EI, Potbury SS, MacGinitie HD (eds) Eocene flora of Western America, vol Nr. 465. Carnegie Institution of Washington Publications, Washington, pp 83–151
Google Scholar
Magain N, Goffinet B, Serusiaux E (2012) Further photomorphs in the lichen family Lobariaceae from Reunion (Mascarene archipelago) with notes on the phylogeny of Dendriscocaulon cyanomorphs. Bryologist 115(2):243–254. https://doi.org/10.2307/23321026
Article Google Scholar
Mägdefrau K (1957) Flechten und Moose im baltischen Bernstein. Ber deutsch Bot Ges 9:433–435
Google Scholar
Malavasi V, Skaloud P, Rindi F, Tempesta S, Paoletti M, Marcella P (2016) DNA-based taxonomy in ecologically versatile microalgae: a re-evaluation of the species concept within the coccoid green algal genus Coccomyxa (Trebouxiophyceae, Chlorophyta). PLoS One 11(3):e0151137. (25 p). https://doi.org/10.1371/journal.pone.0151137
Article CAS Google Scholar
Mara N, Da V, Marinho Pereira T, Astolfi Filho S, Matsuura T (2011) Taxonomic characterization and antimicrobial activity of actinomycetes associated with foliose lichens from the Amazonian ecosystems. Aust J Basic Appl Sci 5:910–918
Google Scholar
Masumoto H (2020) Taxonomic studies on lichenized basidiomycetes and their photobionts in Japan: towards the establishment of a model co-culture system of lichen symbiosis. Ph.D. thesis, University of Tsukuba
Google Scholar
Matsunaga KKS, Stockey RA, Tomescu AMF (2013) Honeggeriella complexa gen. et sp. nov., a heteromerous lichen from the Lower Cretaceous (Valanginian-Hauterivian) of Vancouver Island (British Columbia, Canada). Am J Bot 100(2):450–459. https://doi.org/10.3732/ajb.1200470
Article Google Scholar
McDonogh RS (1939) The habitat, distribution and dispersal of the psycid moth, Luffia ferchaultella, in England and Wales. Anim Ecol 8:10–28
Article Google Scholar
Mehlman P (1988) Food resources of the wild Barbary Macaque Macaca sylvanus in high-altitude fir forest Ghomaran Rif Morocco. J Zool 214(3):469–490. https://doi.org/10.1111/j.1469-7998.1988.tb03754.x
Article Google Scholar
Meier FA, Scherrer S, Honegger R (2002) Faecal pellets of lichenivorous mites contain viable cells of the lichen-forming ascomycete Xanthoria parietina and its green algal photobiont, Trebouxia arboricola. Biol J Linn Soc 76(2):259–268. https://doi.org/10.1111/j.1095-8312.2002.tb02087.x
Article Google Scholar
Merges D, Dal Grande F, Greve C, Otte J, Schmitt I (2021) Virus diversity in metagenomes of a lichen symbiosis (Umbilicaria phaea): complete viral genomes, putative hosts and elevational distributions. Environ Microbiol 23(11):6637–6650. https://doi.org/10.1111/1462-2920.15802
Article CAS Google Scholar
Merinero S, Gauslaa Y (2018) Specialized fungal parasites reduce fitness of their lichen hosts. Ann Bot 121(1):175–182. https://doi.org/10.1093/aob/mcx124
Article CAS Google Scholar
Metz S, Singer D, Domaizon I, Unrein F, Lara E (2019) Global distribution of Trebouxiophyceae diversity explored by high-throughput sequencing and phylogenetic approaches. Environ Microbiol 21(10):3885–3895. https://doi.org/10.1111/1462-2920.14738
Article CAS Google Scholar
Miao V (1999) Molecular diversity of polyketide biosynthesis genes in lichens. In: Baltz RH, Hegeman GD (eds) Developments in industrial microbiology. Society of Industrial Microbiology, pp 57–60
Google Scholar
Millanes AM, Diederich P, Westberg M, Wedin M (2016a) Three new species in the Biatoropsis usnearum complex. Herz 292:337–354. https://doi.org/10.13158/heia.29.2.2016.337
Article Google Scholar
Millanes AM, Diederich P, Wedin M (2016b) Cyphobasidium gen. nov., a new lichen-inhabiting lineage in the Cystobasidiomycetes (Pucciniomycotina, Basidiomycota, Fungi). Fungal Biol 120(11):1468–1477. https://doi.org/10.1016/j.funbio.2015.12.003
Article Google Scholar
Millanes AM, Diederich P, Westberg M, Wedin M (2021) Crittendenia gen. nov., a new lichenicolous lineage in the Agaricostilbomycetes (Pucciniomycotina), and a review of the biology, phylogeny and classification of lichenicolous heterobasidiomycetes. Lichenologist 53(1):103–116. https://doi.org/10.1017/S002428292000033X
Article Google Scholar
Mitchell JC, Champion RH (1965) Human allergy to lichens. Bryologist 68(1):116–118
Article Google Scholar
Moncada B, Perez RE, Lücking R (2019) The lichenized genus Cora (Basidiomycota: Hygrophoraceae) in Mexico: high species richness, multiple colonization events, and high endemism. Plant Fungal Syst 64(2):393–411. https://doi.org/10.2478/pfs-2019-0026
Article Google Scholar
Moncada B, Mercado-Díaz JA, Smith CW et al (2021) Two new common, previously unrecognized species in the Sticta weigelii morphodeme (Ascomycota: Peltigeraceae). Willdenowia 51:35–45. https://doi.org/10.3372/wi.51.51103
Article Google Scholar
Motiejûnaitë J, Jucevièienë N (2005) Epidemiology of the fungus Athelia arachnoidea in epiphytic communities of broadleaved forests under strong anthropogenic impact. Ekologija 4:28–34
Google Scholar
Moya P, Škaloud P, Chiva S et al (2015) Molecular phylogeny and ultrastructure of the lichen microalga Asterochloris mediterranea sp. nov. from Mediterranean and Canary Islands ecosystems. Int J Syst Evol Microbiol 65:1838–1854. https://doi.org/10.1099/ijs.0.000185
Article CAS Google Scholar
Moya P, Molins A, Chiva S, Bastida J, Barreno E (2020) Symbiotic microalgal diversity within lichenicolous lichens and crustose hosts on Iberian Peninsula gypsum biocrusts. Nat Sci Rep 10(Article Nr. 14060):14. doi:https://doi.org/10.1038/s41598-020-71046-2
Muggia L, Baloch E, Stabentheiner E, Grube M, Wedin M (2011) Photobiont association and genetic diversity of the optionally lichenized fungus Schizoxylon albescens. FEMS Microbiol Ecol 75(2):255–272. https://doi.org/10.1111/j.1574-6941.2010.01002.x
Article CAS Google Scholar
Muggia L, Zellnig G, Rabensteiner J, Grube M (2012) Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region. Symbiosis 51(2):149–160. https://doi.org/10.1007/s13199-010-0060-8
Article Google Scholar
Muggia L, Klug B, Berg G, Grube M (2013) Localization of bacteria in lichens from Alpine soil crusts by fluorescence in situ hybridization. Appl Soil Ecol 68:20–25. https://doi.org/10.1016/j.apsoil.2013.03.008
Article Google Scholar
Muggia L, Nelsen MP, Kirika PM et al (2020a) Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus Trebouxia (Trebouxiophyceae, Chlorophyta): An impetus for developing an integrated taxonomy. Mol Phylogenet Evol 149:106821. https://doi.org/10.1016/j.ympev.2020.106821
Article Google Scholar
Muggia L, Zalar P, Azua-Bustos A, González-Silv C, Grube M, Gunde-Cimerman N (2020b) The beauty and the yeast: can the microalgae Dunaliella form a borderline lichen with Hortaea werneckii? Symbiosis 82:123–131. https://doi.org/10.1007/s13199-020-00697-6
Article Google Scholar
Muggia L, Quan Y, Gueidan C, Al-Hatmi AMS, Grube M, Hoog S (2021) Sequence data from isolated lichen-associated melanized fungi enhance delimitation of two new lineages within Chaetothyriomycetidae. Mycol Progr 20:911–927. https://doi.org/10.1007/s11557-021-01706-8
Article Google Scholar
Mushegian AA, Peterson CN, Baker CCM, Pringle A (2011) Bacterial diversity across individual lichens. Appl Environ Microbiol 77:4249–4252. https://doi.org/10.1128/AEM.02850-10
Article CAS Google Scholar
Myers-Smith IH, Forbes BC, Wilmking M et al (2011) Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6(4):045509. (15 p). https://doi.org/10.1088/1748-9326/6/4/045509
Article Google Scholar
Myers-Smith IH, Grabowski MM, Thomas HJD et al (2019) Eighteen years of ecological monitoring reveals multiple lines of evidence for tundra vegetation change. Ecologi. Monogr 89(2):e01351.:21 p. https://doi.org/10.1002/ecm.1351
Article Google Scholar
Nelsen MP, Lücking R, Grube M et al (2009) Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Stud Mycol 64(1):135–144. https://doi.org/10.3114/sim.2009.64.07
Article CAS Google Scholar
Nelsen MP, Lücking R, Boyce CK, Lumbsch HT, Ree RH (2019) No support for the emergence of lichens prior to the evolution of vascular plants. Geobiology: 11. doi: https://doi.org/10.1111/gbi.12369
Nelsen MP, Lücking R, Boyce CK, Lumbsch HT, Ree RH (2020) The macroevolutionary dynamics of symbiotic and phenotypic diversification in lichens. PNAS 117(35):21495–21503. https://doi.org/10.1073/pnas.2001913117
Article CAS Google Scholar
Nicolaou KC, Zhang H, Chen JS, Crawford JJ, Pasunoori L (2007) Total synthesis and stereochemistry of uncialamycin. Angewandte Chemie Internationale Edition 46(25):4704–4707. https://doi.org/10.1002/anie.200700917
Article CAS Google Scholar
Nicolaou KC, Rigol S, Pitsinos EN et al (2021) Uncialamycin-based antibody-drug conjugates: unique enediyne ADCs exhibiting bystander killing effect. PNAS 118(25):e2107042118.:7 p. https://doi.org/10.1073/pnas.2107042118
Article CAS Google Scholar
Nimis PL, Scheidegger C, Wolseley PA (eds) (2002) Monitoring with lichens - monitoring lichens; NATO science series, IV. earth and environmental sciences, vol 7. Springer Science & Business Media, Dordrecht
Google Scholar
Noël A, Garnier A, Clément M et al (2021) Lichen-associated bacteria transform antibacterial usnic acid to products of lower antibiotic activity. Phytochemistry 181:112535. https://doi.org/10.1016/j.phytochem.2020.112535
Article CAS Google Scholar
Noh HJ, Lee YM, Park CH, Lee HK, Cho JC, Hong SG (2020) Microbiome in Cladonia squamosa is vertically stratified according to microclimatic conditions. Front Microbiol 11(article Nr. 268). doi:https://doi.org/10.3389/fmicb.2020.00268
Noorjahan A, Aiyamperumal B, Anantharaman P (2021) Fungal endophytes from seaweeds and bio-potential applications in agriculture. In: Sharma VK, Shah MP, Parmar S, Kumar A (eds) Fungi bio-prospects in sustainable agriculture, environment and nano-technology, volume 1: fungal diversity of sustainable agriculture. Academic, pp 83–95. https://doi.org/10.1016/B978-0-12-821394-0.00003-2
Chapter Google Scholar
Nyati S, Werth S, Honegger R (2013) Genetic diversity of sterile cultured Trebouxia photobionts associated with the lichen-forming fungus Xanthoria parietina visualized with RAPD-PCR fingerprinting techniques. Lichenologist 45(6):825–840. https://doi.org/10.1017/S0024282913000546
Article Google Scholar
Nyati S, Scherrer S, Werth S, Honegger R (2014) Green algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes). Lichenologist 46(2):189–212. https://doi.org/10.1017/S0024282913000819
Article Google Scholar
Olivier-Jimenez D, Chollet-Krugler M, Rondeau D, et al. (2019) A database of high-resolution MS/MS spectra for lichen metabolites. Sci Data 6(1, article Nr. 294); doi: https://doi.org/10.1038/s41597-019-0305-1
Osyczka P, Lenart-Boroń A, Boroń P, Rola K (2020) Lichen-forming fungi in postindustrial habitats involve alternative photobionts. Mycologia 113(1):43–55. https://doi.org/10.1080/00275514.2020.1813486
Article CAS Google Scholar
Ott S, Przewosnik R, Sojo F, Jahns HM (1997) The nature of cephalodia in Placopsis contortuplicatus and other species of the genus. Bibl Lichenol 67:69–84
Google Scholar
Pankratov TA, Grouzdev DS, Patutina EO, Kolganova TV, Suzina NE, Berestovskaya JJ (2020) Lichenibacterium ramalinae gen. nov, sp. nov., Lichenibacterium minor sp. nov., the first endophytic, beta-carotene producing bacterial representatives from lichen thalli and the proposal of the new family Lichenibacteriaceae within the order Rhizobiales. A van Leeuw 113(1):477–489. https://doi.org/10.1007/s10482-019-01357-6
Article CAS Google Scholar
Parrini F, Cain JW, Krausman PR (2009) Capra ibex (Artiodactyla: Bovidae). Mamm Species 830:1–12. https://doi.org/10.1644/830.1
Article Google Scholar
Parrot D, Antony-Babu S, Intertaglia L, Grube M, Tomasi S, Suzuki MT (2015) Littoral lichens as a novel source of potentially bioactive Actinobacteria. Sci Rep 5(15839):14. https://doi.org/10.1038/srep15839
Article CAS Google Scholar
Parrot D, Legrave N, Intertaglia L et al (2016a) Cyaneodimycin, a bioactive compound isolated from the culture of Streptomyces cyaneofuscatus associated with Lichina confinis. Eur J Org Chem 2016:3977–3982. https://doi.org/10.1002/ejoc.201600252
Article CAS Google Scholar
Parrot D, Legrave N, Delmail D, Grube M, Suzuki MT, Tomasi S (2016b) Review – Lichen-associated bacteria as a hot spot of chemodiversity: Focus on uncialamycin, a promising compound for future medicinal applications. Planta Med 82(13):10. https://doi.org/10.1055/s-0042-105571
Article CAS Google Scholar
Paulsrud P, Rikkinen J, Lindblad P (1998) Cyanobiont specificity in some Nostoc-containing lichens and in a Peltigera aphthosa photosymbiodeme. New Phytol 139(3):517–524. https://doi.org/10.1046/j.1469-8137.1998.00220.x
Article CAS Google Scholar
Pegau RE (1970) Succession in two exclosures near Unalakleet, Alaska. Can Field-Nat 84:175–177
Google Scholar
Pérez-Ortega S, Garrido-Benavent I, Grube M, Olmo R, De los Ríos A (2016) Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta). Fungal Divers 80(1):285–300. https://doi.org/10.1007/s13225-016-0361-1
Article Google Scholar
Pérez-Ortega S, Miller KA, Ríos ADI (2018) Challenging the lichen concept: Turgidosculum ulvae (Verrucariaceae) represents an independent photobiont shift to a multicellular blade-like alga. Lichenologist 50(3):341–356. https://doi.org/10.1017/S0024282918000117
Article Google Scholar
Peterson EB (2000) An overlooked fossil lichen (Lobariaceae). Lichenologist 32:289–300. https://doi.org/10.1006/lich.1999.0257
Article Google Scholar
Petrini O, Hake U, Dreyfuss MM (1990) An analysis of fungal communities isolated from fruticose lichens. Mycologia 82:444–451
Article Google Scholar
Petrzik K, Vondrak J, Bartak M, Peksa O, Kubešová O (2013) Lichens—a new source or yet unknown host of herbaceous plant viruses? Eur J Plant Pathol 138(3):11. https://doi.org/10.1007/s10658-013-0246-z
Article CAS Google Scholar
Petrzik K, Vondrak J, Kvíderova J, Lukavský J (2015) Platinum anniversary: virus and lichen alga together more than 70 years. PLoS One 10:1–12. https://doi.org/10.1371/journal.pone.0120768
Article CAS Google Scholar
Petrzik K, Koloniuk I, Sehadova H, Sarkisova T (2019) Chrysoviruses inhabited symbiotic fungi of lichens. Viruses 11(12):1120. https://doi.org/10.3390/v11121120
Article CAS Google Scholar
Picard KT, Letcher PM, Powell MJ (2013) Evidence for a facultative mutualist nutritional relationship between the green coccoid alga Bracteacoccus sp. (Chlorophyceae) and the zoosporic fungus Rhizidium phycophilum (Chytridiomycota). Fungal Biol 117(5):319–328. https://doi.org/10.1016/j.funbio.2013.03.003
Article Google Scholar
Piercey-Normore MD (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytol 169:331–344. https://doi.org/10.1111/j.1469-8137.2005.01576.x
Article CAS Google Scholar
Pino-Bodas R, Stenroos S (2021) Global biodiversity patterns of the photobionts associated with the genus Cladonia (Lecanorales, Ascomycota). Microb Ecol 82(1):1–15. https://doi.org/10.1007/s00248-020-01633-3
Article CAS Google Scholar
Pizarro D, Divakar PK, Grewe F, Crespo A, Dal Grande F, Lumbsch T (2020) Genome-wide analysis of biosynthetic gene cluster reveals correlated gene loss with absence of usnic acid in lichen-forming fungi. Genome Biol Evol 12(10):1858–1868. https://doi.org/10.1093/gbe/evaa189
Article CAS Google Scholar
Poelt J, Huneck S (1968) Lecanora vinetorum nova spec., ihre Vergesellschaftung, ihre Ökologie und ihre Chemie. Osterr Bot Z 115:411–422
Article CAS Google Scholar
Poelt J, Mayrhofer H (1988) Ueber Cyanotrophie bei Flechten. Plant Syst Evol 158:265–281
Article Google Scholar
Poinar GOJ (1994) The range of life in amber: significance and implications in DNA studies. Experientia 50(6):536–542. https://doi.org/10.1007/BF01921722
Article CAS Google Scholar
Poinar GO Jr, Peterson EB, Platt JL (2000) Fossil Parmelia in New World amber. Lichenologist 32(3):263–269. https://doi.org/10.1006/lich.1999.0258
Article Google Scholar
Powell MJ (2017) Chytridiomycota. In: Archibald J, Simpson A, Slamovits C (eds) Handbook of the protists. Springer, Cham, pp 1523–1558. https://doi.org/10.1007/978-3-319-28149-0_18
Chapter Google Scholar
Prieto M, Baloch E, Tehler A, Wedin M (2013) Mazaedium evolution in the Ascomycota (Fungi) and the classification of mazaediate groups of formerly unclear relationship. Cladistics 29(3):296–308. https://doi.org/10.1111/j.1096-0031.2012.00429.x
Article Google Scholar
Prillinger H, Kraepelin G, Lopandic K et al (1997) New species of Fellomyces isolated from epiphytic lichen species. Syst Appl Microbiol 20(4):572–584. https://doi.org/10.1016/S0723-2020(97)80029-X
Article CAS Google Scholar
Rambold G (1985) Fütterungsexperiment mit den an Flechten fressenden Raupen von Setina aurita Esp. (Lep. Arctiidae). NachrBl Bayer Ent 34:82–90. https://www.zobodat.at/pdf/NachBlBayEnt_034_0082-0090.pdf
Google Scholar
Ranft H, Moncada B, de Lange PJ, Lumbsch T, Lücking R (2018) The Sticta filix morphodeme (Ascomycota: Lobariaceae) in New Zealand with the newly recognized species S. dendroides and S. menziesii: indicators of forest health in a threatened island biota? Lichenologist 50(2):185–210. https://doi.org/10.1017/S0024282917000706
Article Google Scholar
Ranković B (ed) (2019) Lichen secondary metabolites, bioactive properties and pharmaceutical potential. Springer Nature Switzerland AG, Cham, p 202
Google Scholar
Reeb V, Lutzoni F, Roux C (2004) Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 32(3):1036–1060. https://doi.org/10.1016/j.ympev.2004.04.012
Article CAS Google Scholar
Resl P, Bujold AR, Tagirdzhanova G et al (2022) Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts. nature research. Nat Commun 13:14. https://doi.org/10.1038/s41467-022-30218-6
Article CAS Google Scholar
Retallack GJ (2009) Cambrian–Ordovician non-marine fossils from South Australia. Alcheringa 33(4):355–391. https://doi.org/10.1080/03115510903271066
Article Google Scholar
Retallack GJ (2020) Ordovician land plants and fungi from Douglas Dam, Tennessee. Palaeobotanist 63(1-2):173–205
Google Scholar
Retallack GJ, Landing E (2014) Affinities and architecture of Devonian trunks of Prototaxites loganii. Mycologia 106(6):1143–1158. https://doi.org/10.3852/13-390
Article CAS Google Scholar
Reutimann P, Scheidegger C (1987) Importance of lichen secondary products in food choice of two oribatid mites (Acari) in an alpine meadow ecosystem. J Chem Ecol 13:363–370. https://doi.org/10.1007/BF01025896
Article CAS Google Scholar
Richardson DHS, Young CM (1977) Lichens and vertebrates. In: Seaward MRD (ed) Lichen ecology. Academic, London, pp 121–144
Google Scholar
Rikkinen J (2003) Calicioid lichens from European Tertiary amber. Mycologia 95(6):1032–1036. https://doi.org/10.1080/15572536.2004.11833019
Article Google Scholar
Rikkinen J, Poinar GOJ (2002) Fossilised Anzia (Lecanorales, lichenforming Ascomycota) from European Tertiary amber. Mycol Res 106:984–990. https://doi.org/10.1017/S0953756202005907
Article Google Scholar
Rikkinen J, Poinar GO (2008) A new species of Phyllopsora (Lecanorales, lichen-forming Ascomycota) from Dominican amber, with remarks on the fossil history of lichens. J Exp Bot 59(5):1007–1011. https://doi.org/10.1093/jxb/ern004
Article CAS Google Scholar
Rikkinen J, Meinke SKL, Grabenhorst H et al (2018) Calicioid lichens and fungi in amber – Tracing extant lineages back to the Paleogene. Geobios 51(5):469–479. https://doi.org/10.1016/j.geobios.2018.08.009
Article Google Scholar
Romano I, Ventorino V, Pepe O (2020) Effectiveness of plant beneficial microbes: Overview of the methodological approaches for the assessment of root colonization and persistence. Front Plant Sci 11(6):16. https://doi.org/10.3389/fpls.2020.00006
Article Google Scholar
Rosentreter R, Eslick L (1993) Notes on the Bryorias used by flying squirrels for nest construction. Evansia 10(2):61–63
Article Google Scholar
Rosentreter R, Hayward GD, Wicklow-Howard M (1997) Northern flying squirrel seasonal food habits in the interior conifer forests of Central ldaho, USA. Northwest Sci 71(2):97–102
Google Scholar
Sanders WB, Masumoto H (2021) Lichen algae: the photosynthetic partners in lichen symbioses. Lichenologist 53(5):347–393. https://doi.org/10.1017/S0024282921000335
Article Google Scholar
Sanders WB, Pérez-Ortega S, Nelsen MP, Lücking R, De los Ríos A (2016) Heveochlorella (Trebouxiophyceae): a little-known genus of unicellular green algae outside the Trebouxiales emerges unexpectedly as a major clade of lichen photobionts in foliicolous communities. J Phycol 52(5):840–853. https://doi.org/10.1111/jpy.12446
Article CAS Google Scholar
Saniewski M, Wietrzyk-Pełka P, Zalewska T, Olech M, Węgrzyn MH (2020) Bryophytes and lichens as fallout originated radionuclide indicators in the Svalbard archipelago (High Arctic). Pol Sci 25(article Nr. 100536):6 DOI: https://doi.org/10.1016/j.polar.2020.100536
Šatkauskienė I (2012) Microfauna of lichen (Xanthoria parietina) in Lithuania: diversity patterns in polluted and non-polluted sites. Baltic For 18(2):255–262
Google Scholar
Scheidegger C, Schroeter B, Frey B (1995) Structural and functional processes during water vapour uptake and desiccation in selected lichens with green algal photobionts. Planta 197(2):399–409. https://doi.org/10.1007/BF00202663
Article CAS Google Scholar
Scherrer S, Honegger R (2003) Inter- and intraspecific variation of homologous hydrophobin (H1) gene sequences among Xanthoria spp. (lichen-forming ascomycetes). New Phytol 158(2):375–389. https://doi.org/10.1046/j.1469-8137.2003.00740.x
Article CAS Google Scholar
Scherrer S, De Vries OMH, Dudler R, Wessels JGH, Honegger R (2000) Interfacial self-assembly of fungal hydrophobins of the lichen-forming ascomycetes Xanthoria parietina and X. ectaneoides. Fungal Gen Biol 30(1):81–93. https://doi.org/10.1006/fgbi.2000.1205
Article CAS Google Scholar
Scherrer S, Haisch A, Honegger R (2002) Characterization and expression of XPH1, the hydrophobin gene of the lichen-forming ascomycete Xanthoria parietina. New Phytol 154(1):175–184. https://doi.org/10.1046/j.1469-8137.2002.00351.x
Article CAS Google Scholar
Scherrer S, Zippler U, Honegger R (2005) Characterisation of the mating-type locus in the genus Xanthoria (lichen-forming ascomycetes, Lecanoromycetes). Fungal Gen Biol 42:976–988. https://doi.org/10.1016/j.fgb.2005.09.002
Article CAS Google Scholar
Schmidt AR, Dörfelt H, Grabenhorst H, Tuovila H, Rikkinen J (2013) Fungi of the Bitterfeld amber forest. Exkurs f und Veröfftl DGG 249:54–60. https://core.ac.uk/reader/286389747
Google Scholar
Schmidt AR, Steuernagel L, Behling H et al (2022) Fossil evidence of lichen grazing from Paleogene amber. Rev Palaeobot Palynol 302(104664):10. https://doi.org/10.1016/j.revpalbo.2022.104664
Article Google Scholar
Schmitt I, Lumbsch HT (2009) Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS One 4(2):e4437., 8 p. https://doi.org/10.1371/journal.pone.0004437
Article CAS Google Scholar
Schroeckh V, Scherlach K, Nützmann H-W et al (2009) Intimate bacterial–fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. PNAS 106(34):14558–14563. https://doi.org/10.1073/pnas.0901870106
Article Google Scholar
Schüssler A (2012) The Geosiphon–Nostoc endosymbiosis and its role as a model for arbuscular mycorrhiza research. In: Hock B (ed) Fungal associations, The Mycota, vol 9. Springer, Berlin, pp 77–91
Chapter Google Scholar
Schüssler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936. https://doi.org/10.1038/nature05364
Article CAS Google Scholar
Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2007) Arbuscular Mycorrhiza. Studies on the Geosiphon symbiosis lead to the characterization of the first glomeromycotan sugar transporter. Plant Signal Behav 2(5):431–434. https://doi.org/10.4161/psb.2.5.4465
Article Google Scholar
Schwendener S (1867) Ueber die wahre Natur der Flechtengonidien. Verh Schweiz Naturforsch Ges 51:88–90
Google Scholar
Schwendener S (1869) Die Algentypen der Flechtengonidien. Programm für die Rectoratsfeier der Universität. Universitätsbuchdruckerei C. Schultze, Basel, 42 p & 3 plates
Google Scholar
Seaward MRD (2002) Lichens as monitors of radioelements. In: Nimis PL, Scheidegger C, Wolseley PA (eds) Monitoring with lichens - monitoring lichens; NATO science series, IV earth and environmental sciences, vol 7. Springer Science & Business Media, Dordrecht, pp 85–95
Chapter Google Scholar
Segerer AH (2009) Die Bedeutung von Flechten als Nahrungsquelle für Tiere, insbesondere Schmetterlinge [The role of lichens as food resources for animals, especially Lepidoptera]. Ökologische Rolle der Flechten, Rundgespräche der Kommission für Ökologie 36. Verlag Dr. Freiderich Pfeil, München, pp 109–128
Google Scholar
Selosse MA, Strullu-Derrien C (2015) Origins of the terrestrial flora: A symbiosis with fungi? BIO Web of Conferences 4(Article Nr. 0009):12 p. doi: https://doi.org/10.13140/RG.2.1.2337.7122
Sharnoff S (1998) Lichens and Invertebrates: a brief review and bibliography. https://www.sharnoffphotos.com/lichen_info/invertebrates.html
Sharnoff S, Rosentreter R (1998) Lichen use by wildlife in North America. Lichens of North America Information. https://www.sharnoffphotos.com/lichen_info/fauna.html
Sierra MA, Danko DC, Sandoval TA et al (2020) The microbiomes of seven lichen genera reveal host specificity, a reduced core community and potential as source of antimicrobials. Front Microbiol 11(398):12. https://doi.org/10.3389/fmicb.2020.00398
Article Google Scholar
Sigurbjornsdottir MA, Heiðmarsson S, Jónsdóttir AR, Vilhelmsson O (2014) Novel bacteria associated with Arctic seashore lichens have potential roles in nutrient scavenging. Can J Microbiol 60(5):307–317. https://doi.org/10.1139/cjm-2013-0888
Article CAS Google Scholar
Singh G, Kukwa M, Grande FD, Łubek A, Otte J, Schmitt I (2019) A glimpse into genetic diversity and symbiont interaction patterns in lichen communities from areas with different disturbance histories in Białowieża forest, Poland. Microorganisms 7(335):17. https://doi.org/10.3390/microorganisms7090335
Article CAS Google Scholar
Singh G, Calchera A, Merges D, Grande FD (2022) A candidate gene cluster for the bioactive natural product gyrophoric acid in lichen-forming fungi. doi:https://doi.org/10.1101/2022.01.14.475839
Škaloud P, Peksa O (2008) Comparative study of chloroplast morphology and ontogeny in Asterochloris (Trebouxiophyceae, Chlorophyta). Biologia 3:869–876. https://doi.org/10.2478/s11756-008-0115-y
Article CAS Google Scholar
Škaloud P, Steinova J, Ridka T, Vancurova L, Peksa O (2015) Assembling the challenging puzzle of algal biodiversity: species delimitation within the genus Asterochloris (Trebouxiophyceae, Chlorophyta). J Phycol 51:507–527. https://doi.org/10.1111/jpy.12295
Article CAS Google Scholar
Škaloud P, Friedl T, Hallmann C, Beck A, Grande FD (2016) Taxonomic revision and species delimitation of coccoid green algae currently assigned to the genus Dictyochloropsis (Trebouxiophyceae, Chlorophyta). J Phycol 52(4):599–617. https://doi.org/10.1111/jpy.12422
Article CAS Google Scholar
Skinner J (2021) Some observations on mollusc damage to lichens. Brit Lichen Soc Bull 129:8–16
Google Scholar
Skubała P, Rola K, Osyczka P, Kafel AI (2014) Oribatid mite communities on lichens in heavily contaminated post-smelting dumps. Arch Environ Con Tox 67(4):578–592. https://doi.org/10.1007/s00244-014-0066-y
Article CAS Google Scholar
Škvorová Z, Černajová I, Steinová J, Peksa O, Moya P, Škaloud P (2022) Promiscuity in lichens follows clear rules: partner switching in Cladonia is regulated by climatic factors and soil chemistry. Front Microbiol 12(article Nr. 781585):15. https://doi.org/10.3389/fmicb.2021.781585
Article Google Scholar
Slocum RD, Lawrey JD (1976) Viability of the epizoic lichen flora carried and dispersed by green lacewing (Nodita pavida) larvae. Can J Bot 54:1827–1831. https://doi.org/10.1139/b76-196
Article Google Scholar
Solhaug KA, Lind M, Nybakken L, Gauslaa Y (2009) Possible functional roles of cortical depsides and medullary depsidones in the foliose lichen Hypogymnia physodes. Flora 204:40–48. https://doi.org/10.1016/j.flora.2007.12.002
Article Google Scholar
Spribille T, Resl P, Ahti T et al (2014) Molecular systematics of the wood-inhabiting, lichen-forming genus Xylographa (Baeomycetales, Ostropomycetidae) with eight new species. Acta Univ Ups Symb Bot Ups 37(1):8–87
Google Scholar
Spribille T, Tuovinen V, Resl P et al (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492. https://doi.org/10.1126/science.aaf8287
Article CAS Google Scholar
Stahl E (1877) Ueber die Bedeutung der Hymenialgonidien. Beiträge zur Entwickelungsgeschichte der Flechten, Heft II. Arthur Felix, Leipzig, p 32
Book Google Scholar
Stahl E (1904) Die Schutzmittel der Flechten gegen Tierfrass. Festschrift zum siebzigsten Geburtstage von Ernst Haeckel. Fischer, Jena, pp 357–375
Google Scholar
Stein WE, Harmon GD, Hueber FM (1993) Spongiophyton from the Lower Devonian of North America reinterpreted as a lichen. Am J Bot 80(6):93
Google Scholar
Stewart A, Rioux D, Boyer F, et al. (2021) Altitudinal zonation of green algae biodiversity in the French Alps Front Plant Sci 12(article Nr. 679428):17 p. doi: https://doi.org/10.3389/fpls.2021.679428
Stocker-Wörgötter E (1995) Experimental cultivation of lichens and lichen symbionts. Can J Bot 73:S579–S589. https://doi.org/10.1139/b95-298
Article Google Scholar
Stocker-Wörgötter E, Cordeiro LMC, Iacomini M (2013) Accumulation of potential pharmaceutically relevant lichen metabolites in lichens and cultured lichen symbionts. Stud Nat Prod Chem 39:337–380. https://doi.org/10.1016/B978-0-444-62615-8.00010-2
Article CAS Google Scholar
Stoll A, Brack A, Renz J (1947) Die antibakterielle Wirkung der Usninsäure auf Mykobakterien und andere Mikroorganismen. Experientia 3(3):115–117
Article CAS Google Scholar
Strother PK, Wellman CH (2016) Palaeoecology of a billion-year-old non-marine cyanobacterium from the Torridon Group and Nonesuch Formation. Palaeontology 59:89–108. https://doi.org/10.1111/pala.12212
Article Google Scholar
Stubbs CS (1989) Patterns of distribution and abundance of corticolous lichens and their invertebrate associates on Quercus rubra in Maine. Bryologist 92(4):453–460
Article Google Scholar
Stubbs CS (1995) Dispersal of soredia by the oribatid mite, Humerobates arborea. Mycologia 87(4):454–458
Article Google Scholar
Studzinska-Sroka E, Galanty A, Bylka W (2017) Atranorin - an interesting lichen secondary metabolite. Mini Rev Med Chem 17(17):1633–1645. https://doi.org/10.2174/1389557517666170425105727
Article CAS Google Scholar
Suzuki MT, Parrot D, Berg G, Grube M, Tomasi S (2016) Lichens as natural sources of biotechnologically relevant bacteria. Appl Microbiol Biotech 100(2):583–595. https://doi.org/10.1007/s00253-015-7114-z
Article CAS Google Scholar
Sveshnikova N, Piercey-Normore MD (2021) Transcriptome comparison of secondary metabolite biosynthesis genes expressed in cultured and lichenized conditions of Cladonia rangiferina. Diversity 13(11, article Nr. 529): 17 p. doi: https://doi.org/10.3390/d13110529
Taylor TN, Hass H, Remy W, Kerp H (1995) The oldest fossil lichen. Nature 378(6554):244. https://doi.org/10.1038/378244a0
Article CAS Google Scholar
Taylor T, Hass H, Kerp H (1997) A cyanolichen from the Lower Devonian Rhynie Chert. Am J Bot 84:992–1004. https://doi.org/10.2307/2446290
Article CAS Google Scholar
Taylor WA, Free C, Boyce C, Helgemo R, Ochoada J (2004) SEM analysis of Spongiophyton interpreted as a fossil lichen. Int J Plant Sci 165(5):875–881. https://doi.org/10.1086/422129
Article Google Scholar
ten Veldhuis M-C, Ananyev G, Dismukes GC (2019) Symbiosis extended: exchange of photosynthetic O₂ and fungal-respired CO₂ mutually power metabolism of lichen symbionts. Photosynth Res 143:287–299. https://doi.org/10.1007/s11120-019-00702-0
Article CAS Google Scholar
Théau J, Peddle DR, Duguay CR (2005) Mapping lichen in a caribou habitat of Northern Quebec, Canada, using an enhancement-classification method and spectral mixture analysis. Remote Sens Environ 94:232–243. https://doi.org/10.1016/j.rse.2004.10.008
Article Google Scholar
Thomas EA (1939) Ueber die Biologie von Flechtenbildnern. Beitr Kryptogamenflora Schweiz 9:1–108
Google Scholar
Tønsberg T, Blom H, Goffinet B, Holtan-Hartwig J, Lindblom L (2016) The cyanomorph of Ricasolia virens comb. nov. (Lobariaceae, lichenized Ascomycetes). Opuscula Philolichenum 15:12–21
Google Scholar
Toxopeus J, Kozera CJ, O'Leary SJB, Garbary DJ (2011) A reclassification of Mycophycias ascophylli (Ascomycota) based on nuclear large ribosomal subunit DNA sequences. Bot Mar 54(3):325–334. https://doi.org/10.1515/bot.2011.032
Article Google Scholar
Trembley ML, Ringli C, Honegger R (2002a) Hydrophobins DGH1, DGH2, and DGH3 in the lichen-forming basidiomycete Dictyonema glabratum. Fungal Genet Biol 35(3):247–259. https://doi.org/10.1006/fgbi.2001.1325
Article CAS Google Scholar
Trembley ML, Ringli C, Honegger R (2002b) Differential expression of hydrophobins DGH1, DGH2 and DGH3 and immunolocalization of DGH1 in strata of the lichenized basidiocarp of Dictyonema glabratum. New Phytol 154(1):185–195. https://doi.org/10.1046/J.1469-8137.2002.00360.X
Article CAS Google Scholar
Tripathi M, Joshi Y (2019) Endolichenic fungi: A promising source for novel bioactive compounds. In: Tripathi M, Joshi Y (eds) Endolichenic fungi: present and future trends. Springer Nature Singapore Pte Ltd, Singapore, pp 69–118. https://doi.org/10.1007/978-981-13-7268-1_5
Chapter Google Scholar
Tschermak-Woess E (1988) The algal partner. In: Galun M (ed) Handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 39–92
Google Scholar
Tuovinen V, Ekman S, Thor G, Vanderpool D, Spribille T, Johannesson H (2019) Two basidiomycete fungi in the cortex of wolf lichens. Curr Biol 29(3):476–483. https://doi.org/10.1016/j.cub.2018.12.022
Article CAS Google Scholar
Tuovinen V, Millanes AM, Freire Rallo S, Rosling A, Wedin M (2021) Tremella macrobasidiata and Tremella variae have abundant and widespread yeast stages in Lecanora lichens. Environ Microbiol 23(5):16. https://doi.org/10.1111/1462-2920.15455
Article CAS Google Scholar
U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch A, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914. https://doi.org/10.3732/ajb.1100459
Article Google Scholar
Urayama S-i, Doi N, Kondo F, et al. (2020) Diverged and active partitiviruses in lichen. Front Microbiol 11(article Nr. 561344): 8. doi: https://doi.org/10.3389/fmicb.2020.561344
U'Ren JM, Lutzoni F, Miadlikowska J, Arnold AE (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 60(2):340–353. https://doi.org/10.1007/s00248-010-9698-2
Article Google Scholar
Ureña-Vacas I, González-Burgos E, Divakar PK, Gómez-Serranillos MP (2021) Lichen depsidones with biological interest. Planta Med 2021:26 pp. https://doi.org/10.1055/a-1482-6381
Vainio EJ, Chiba S, Ghabrial SA et al (2018) ICTV virus taxonomy profile: Partitiviridae. J Gen Virol 99(1):17–18. https://doi.org/10.1099/jgv.0.000985
Article CAS Google Scholar
Van Beneden PJ (1875) Les commensaux et les parasites. Biblio Sci Int, Paris, 284 p. https://gallica.bnf.fr/ark:/12148/bpt6k1170287z.image
Van den Wyngaert S, Rojas-Jimenez K, Seto K, Kagami M, Grossart H-P (2018) Diversity and hidden host specificity of chytrids infecting colonial volvocacean algae. J Eukaryot Microbiol 65(6):870–881. https://doi.org/10.1111/jeu.12632
Article CAS Google Scholar
Vanderduys E (2012) Field guide to the frogs of Queensland. CSIRO Publishing, Collingwood, p 72
Book Google Scholar
Wang X, Krings M, Taylor TN (2010) A thalloid organism with possible lichen affinity from the Jurassic of northeastern China. Rev Palaeobot Palynol 162(4):591–598. https://doi.org/10.1016/j.revpalbo.2010.07.005
Article Google Scholar
Wang Y, Wang J, Cheong YH, Hur JS (2014) Three new non-reducing polyketide synthase genes from the lichen-forming fungus Usnea longissima. Mycobiology 42(1):34–40. https://doi.org/10.5941/MYCO.2014.42.1.34
Article CAS Google Scholar
Wang Y, Zhao N, Yuan XL, Hua M, Hur JS, Yang YM et al (2016) Heterologous transcription of a polyketide synthase gene from the lichen forming fungi Usnea longissima. Res J Biotech 11:16–21
Google Scholar
Warshan D, Espinoza JL, Stuart RK et al (2017) Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant-cyanobacteria symbiosis. ISME J 11(12):2821–2833. https://doi.org/10.1038/ismej.2017.134
Article Google Scholar
Wedin M, Döring H, Gilenstam G (2004) Saprotrophy and lichenization as options for the same fungal species on different substrata: environmental plasticity and fungal lifestyles in the Stictis-Conotrema complex. New Phytol 164:459–468. https://doi.org/10.1111/j.1469-8137.2004.01198.x
Article Google Scholar
Wedin M, Döring H, Könberg K, Gilenstam G (2005) Generic delimitations in the family Stictidaceae (Ostropales, Ascomycota): The Stictis-Conotrema problem. Lichenologist 37(1):67–75. https://doi.org/10.1017/S0024282904014653
Article Google Scholar
Wedin M, Maier S, Fernandez-Brime S, Cronholm B, Westberg M, Grube M (2016) Microbiome change by symbiotic invasion in lichens. Environ Microbiol 18(5):1428–1439. https://doi.org/10.1111/1462-2920.13032
Article CAS Google Scholar
Wessels JGH (1997) Hydrophobins: Proteins that change the nature of the fungal surface. Adv Miocrob Physiol 38:1–45. https://doi.org/10.1016/s0065-2911(08)60154-x
Article CAS Google Scholar
West NJ, Parrot D, Fayet C, Grube M, Tomasi S, Suzuki MT (2018) Marine cyanolichens from different littoral zones are associated with distinct bacterial communities. Peer J 6(e5208):29. https://doi.org/10.7717/peerj.5208
Article CAS Google Scholar
Wethalawe AN, Alwis YV, Udukala DN, Paranagama PA (2021) Antimicrobial compounds isolated from endolichenic fungi: a review. Molecules 26(article Nr. 3901):17. doi:https://doi.org/10.3390/molecules26133901
Wijayawardene NN, Hyde KDA-AL, Tedersoo L, Haelewaters D, Rajeshkumar KC, Zhao RLAA, Leontyev DV, Saxena RK, Tokarev YS, Dai DQ, Letcher PM, Stephenson SL et al (2020) Outline of fungi and fungus-like taxa. Mycosphere 11(1):1060–1456. https://doi.org/10.5943/mycosphere/11/1/8
Article Google Scholar
Wösten HAB (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646. https://doi.org/10.1146/annurev.micro.55.1.625
Article Google Scholar
Wösten HAB, De Vries OMH, Wessels JGH (1993) Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5(11):1567–1574. https://doi.org/10.1105/tpc.5.11.1567
Article Google Scholar
Xiang Z (2014) Rhinopithecus bieti at Xiaochangdu, Tibet: Adaptations to a marginal environment. In: Grow NB, Gursky-Doyen S, Krzton A (eds) High altitude primates developments in primatology: Progress and prospects, vol 44. Springer, pp 183–197. https://doi.org/10.1007/978-1-4614-8175-1_10
Chapter Google Scholar
Xiang Z-F, Grueter CC (2007) First direct evidence of infanticide and cannibalism in wild snub-nosed monkeys (Rhinopithecus bieti). Am J Primatol 69(3):249–254. https://doi.org/10.1002/ajp.20333
Article Google Scholar
Xiang Z-F, Huo S, Xiao W, Quan R-C, Grueter CC (2007) Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: adaptations to a marginal environment. Am J Primatol 69:1141–1158. https://doi.org/10.1002/ajp.20412
Article Google Scholar
Xu H, Deckert RJ, Garbary DJ (2008) Ascophyllum and its symbionts. X. Ultrastructure of the interaction between A. nodosum (Phaeophyceae) and Mycophycias ascophylli (Ascomycetes). Botany 86(2):185–193. https://doi.org/10.1139/B07-122
Article Google Scholar
Xu M, Oppong-Danquah E, Wang X, et al. (2022) Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens. Phytochemistry 200 (article Nr. 113210): pre-print; doi: https://doi.org/10.1016/j.phytochem.2022.113210
Yamamoto Y, Mizugichi R, Yamada Y (1985) Tissue cultures of Usnea rubescens and Ramalina yasudae and production of usnic acid in their cultures. Agric Biol Chem 49:3347–3348. https://doi.org/10.1271/bbb1961.49.3347
Article CAS Google Scholar
Yang B, Zhang P, Garber PA, Hedley R, Li B (2016) Sichuan Snub-Nosed Monkeys (Rhinopithecus roxellana) consume cicadas in the Qinling Mountains, China. Folia Primatol 87:11–16. https://doi.org/10.1159/000443733
Article Google Scholar
Yang Y, Bhosle SR, Yu YH, et al. (2018) Tumidulin, a lichen secondary metabolite, decreases the stemness potential of colorectal cancer cells. 23(11), article Nr. 2968:13 p; doi:https://doi.org/10.3390/molecules23112968
Yang Y, Groves C, Garber P et al (2019) First insights into the feeding habits of the critically endangered black snub-nosed monkey, Rhinopithecus strykeri (Colobinae, Primates). Primates 60(1):11. https://doi.org/10.1007/s10329-019-00717-0
Article Google Scholar
Yockney IJ, Hickling GJ (2000) Distribution and diet of chamois (Rupicapra rupicapra) in Westland forests, South Island, New Zealand. New Zeal. J Ecol 24(1):31–38. https://www.jstor.org/stable/24054648
Google Scholar
Yoshino K, Yamamoto K, Masumoto H et al (2020) Polyol-assimilation capacities of lichen-inhabiting fungi. Lichenologist 52(1):49–59. https://doi.org/10.1017/S0024282919000483
Article Google Scholar
Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020. https://doi.org/10.1126/science.1111347
Article CAS Google Scholar
Zawierucha K, Węgrzyn M, Ostrowska M, Wietrzyk P (2017) Tardigrada in Svalbard lichens: diversity, densities and habitat heterogeneity. Polar Biol 40:1385–1392. https://doi.org/10.1007/s00300-016-2063-2
Article Google Scholar
Zhang Y, Clancy J, Jensen J, McMullin RT, Wang L, Leavitt SD (2022) Providing scale to a known taxonomic unknown—at least a 70-fold increase in species diversity in a cosmopolitan nominal taxon of lichen-forming fungi. J Fungi 8(5, article Nr. 490):18 p. doi: https://doi.org/10.3390/jof8050490
Ziegler R (2001) Fossiler Pflanzenmoder aus dem Keuper. Documenta Naturae 112:1–64
Google Scholar
Zimmermann E, Feusi S (2018) Bemerkenswerte Funde lichenicoler Pilze anlässlich der BRYOLICH-Jahresversammlung 2017 in der Lenk (Berner Oberland, Schweiz). Meylania 61:38–46
Google Scholar
Zimmermann E, Feusi S (2020) Lichenicole Pilze der Schweiz III: Zur Biodiversität lichenicoler Pilze im Engadin (Graubünden, Schweiz). Meylania 66:31–39
Google Scholar
Zopf W (1896) Zur biologischen Bedeutung der Flechtensäuren. Biol Centralbl 16:593–610
Google Scholar
Zopf W (1907) Die Flechtenstoffe in chemischer, botanischer, pharmakologischer und technischer Beziehung. Gustav Fischer Verlag, Jena
Google Scholar

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Acknowledgements

My sincere thanks are due to Prof. Dianne Edwards for fruitful collaboration on fossils, William Bruzgul, Paul Diederich and Robert Lücking for valuable informations, to Andreas Valls for IT support, to Erik Adams, Andrea Bernecker, Joël Boustie, Paul Diedrich, Pierre Le Pogam, Fabio Nodari, Jim Petranka, David Weiller and Erich Zimmermann for permission to include their photos, to Prof. Ueli Grossniklaus, director of the Institute of Plant and Microbial Biology of the University of Zurich, for access to the infrastructure of the institute far beyond my retirement, IT support by Stefan Roffler included. Last but not least, I thank Barry Scott and Carl Mesarich, editors of this volume, for their kind interest, patience and help.

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Institute of Plant and Microbiology, University of Zürich, Zürich, Switzerland
Rosmarie Honegger

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School of Natural Sciences, Massey University, Palmerston North, New Zealand
Barry Scott
School of Agriculture and Environment, Massey University, Palmerston North, New Zealand
Carl Mesarich

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Honegger, R. (2023). Lichens and Their Allies Past and Present. In: Scott, B., Mesarich, C. (eds) Plant Relationships. The Mycota, vol 5. Springer, Cham. https://doi.org/10.1007/978-3-031-16503-0_6

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