Keywords

7.1 Introduction

Yeasts inhabit many ecological niches and, like filamentous fungi, can be isolated from almost every habitat worldwide. As heterotrophs, they rely on different biologically accessible nutrients but are mainly limited in their growth by carbohydrate and nitrogen resources, whereas most other elements are not limiting factors in most habitats. Many fungi have solved the problem of nutrient availability by interacting with other organisms. This has been implicated as one of the reasons for high species diversity in fungi, and especially plant-fungus interaction might have played a key role in the early radiation of fungi (Redecker et al. 2000; Begerow et al. 2004). But fungal interactions are not restricted to plants, and fungi interact with many eukaryotic lineages, including prokaryotes, several protist lineages, plants, and animals. The spectrum of interactions range from neutralism, commensalism, and mutualism to parasitism (e.g., Starmer and Lachance 2011) and are reviewed in other chapters of this book. Here, we will focus on parasitism of yeasts and yeast-like organisms (Fig. 7.1). Reviewing the broad literature, we have to acknowledge that the terms “parasite” and “pathogen” are not clearly separated in the various fields of research. While “pathogen” is broadly used in plant-centered publications, animal literature seem to have a preference for “parasite.” In general, the term “pathogen” is emphasizing the causal agent of a disease, and the term “parasite” is highlighting the form of interaction. Without neglecting the difference between the two terms, we decided to use “parasite” throughout the text for simplicity.

Fig. 7.1
figure 1

Pathogenic stages of yeasts. (a) Oral thrush caused by Candida albicans (Photo: CDC and PHIL © CC-BY-SA 2.0). (b) X-ray of the thorax reveals the telltale signs of non-encapsulated pulmonary cryptococcosis in a patient infected with Cryptococcus sp. (Photo: Centers for Disease Control (CDC) and Prevention’s Public Health Image Library (PHIL) © CC-BY-SA 2.0). (c) Posterior view of a man’s torso reveals the presence of a patchy, erythematous rash caused by Malassezia furfur (Photo: CDC/Dr. Lucille K. Georg © CC-BY-SA 2.0). (d) Peach leaf curl caused by Taphrina deformans (Photo: Giancarlo Dessì © CC-BY-SA 2.0). (e) Protomyces macrosporus gall as seen on the lower surface of Aegopodium podagraria (Photo: Roger Griffith © public domain). (f) Mycosarcoma (Ustilago) maydis sporulating in tumors substituting fruits of Zea mays (Photo: Domink Begerow). (g) Microbotryum lychnidis-dioicae sporulating on the anthers of Silene latifolia (Photo: Angela Schäfer). (h) Various stages of Sterigmatosporidium polymorphum including conidiophores, basidia, hyphae with clamp connections, and tremelloid haustoria from yeasts cells and hyphae (Modified from Kirschner et al. 2001). (i) Sectional view of Cryptomycocolax abnorme including basidia, parasitic hyphae with clamp connections, host cells, and botryose structures of interaction (F. Oberwinkler as published in Oberwinkler and Bauer 1990)

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A major character of yeasts, which has been always stressed in research, is their ability to grow on artificial media. Therefore, their saprobic capabilities (e.g., spectrum of utilized compounds) have been in focus for a long time (reviewed in Barnett 2004). In the middle of the nineteenth century, yeasts were recognized as living organisms and assigned to fungi (Barnett 1998). The first described yeast species originated from fermenting products, a substrate where they often occur in a single-celled form. It is however well accepted nowadays that “yeast” represents a live stage or live form (characterized by singe cells proliferating by budding or fission) that has evolved early in fungal evolution and has been retained in several phylogenetic lineages (Nagy et al. 2014). In many lineages, it represents the only growth form the fungus can exhibit, but researchers have observed filamentous fungi or their spores giving rise to cultures proliferating as yeasts by cell budding. Under certain conditions, yeast-like states could be observed in molds (e.g., Mucor and Penicillium), parasitic ascomycetes (e.g., Taphrina and Kabatiella), jelly fungi (e.g., Auriculariales, Dacrymycetales, Tremellales), and smuts (e.g., Ustilago). Yeast stages of the intensively studied smut fungi were regularly observed and used in experiments, even though budding yeast state was not characterized or explicitly mentioned in the descriptions.

The term “dimorphic”, a term introduced by Brefeld in the 1880s (reviewed in Bandoni 1995), was used to contrast the yeast stage of basidiomycetous fungi having also a dikaryotic hyphal phase from the typical unicellular morphology of ascomycetous yeasts. The life histories of most dimorphic taxa consist of mating of compatible (heterothallic) yeast states to produce dikaryotic mycelia. Haploid conidial development can again result in a yeast state, as it may direct budding of basidia in some taxa. The presence or absence of haploid and/or diploid conidia is a common variation in the life histories (Bandoni 1995). Variations in mating systems are also common, and homothallism is present in some species (e.g., Lin and Heitman 2007; David-Palma et al. 2016).

Fungal parasites of plants were among the first organisms where understanding the role of resting structures and saprobic asexual states in survival and dispersal was achieved. Even though the ability to produce a yeast stage was often viewed from the perspective of systematics rather than from its functional side, mycologists accumulated substantial numbers of examples of parasitic fungi with predominantly unicellular (or yeast-like) asexual states. Most of our present knowledge about so-called heterobasidiomycetes and dimorphic fungi is coming from the research made by Robert J. Bandoni (University of British Columbia, Canada) and Franz Oberwinkler (University of Tübingen, Germany) with collaborators. More recent studies on yeasts in their natural habitats showed complex interactions with the environment, their vectors, and hosts (reviewed by Starmer and Lachance 2011).

Dimorphism is often associated with a change in nutrient acquisition, whereby the yeast stage grows saprobically and the hyphal phase is parasitic. As detailed in this chapter, this behavior has evolved in various lineages and is independent of the host’s phylogenetic position. Especially sequencing technologies and molecular identification (e.g., Begerow et al. 2010; Schoch et al. 2012) have made it possible to recognize the link between yeast and parasitic stages in several lineages, thereby changing our understanding of yeast biology in many ways (Begerow et al. 2014; Begerow and Kemler 2017). Subsequent studies showed that many known basidiomycete yeasts are phylogenetically related to parasitic fungi (Fell et al. 2000; Scorzetti et al. 2002; Liu et al. 2015; Wang et al. 2015a, b).

Recent advances in high-throughput DNA sequencing of fungi showed the potential to develop yeast type of proliferation being widely distributed across Fungi (Nagy et al. 2014). This ability arose early in fungal evolution and became dominant independently in different phylogenetic groups being, possibly, results from the diversification of the gene family (Zn-cluster transcription factors) that are responsible for yeast-filamentous switches (Nagy et al. 2014). Although the transition between filamentous and yeast growth forms (morphs) has been known for more than a century, the importance and role of this adaptation in Fungi are still a matter of scientific debates.

Below we review the knowledge about yeasts as parasites; focus on animal, plants, and fungi as hosts; and follow a phylogenetic approach within each of three ecological groups (Fig. 7.2). However, yeasts associated with humans and invertebrates are discussed in more detail elsewhere (see Chap. 8 of this book and Blackwell 2017, respectively) and therefore are mentioned only briefly. As the majority of our knowledge on parasitism of yeasts is probably based on studies of dimorphic Basidiomycota in the Ustilaginomycotina and some lineages of Pucciniomycotina, these will be reviewed extensively. Where possible, we additionally provide an overview on parasitic stages of fungi in their yeast stage.

Fig. 7.2
figure 2

Overview of the phylogeny of Dikarya including yeast lineages with known parasitic interactions. Fungal genera with yeast states reported as parasites of animals (red, see Sect. 7.2), plants (green, see Sect. 7.3), and other fungi, including lichens (black, see Sect. 7.4)

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7.2 Animal and Human Hosts

With respect to ecology and growth optima, many yeast species are saprobic and mesophilic (Lachance and Starmer 1998). Although yeasts grow as soon as carbohydrates and nitrogen are available, they do not cope well with elevated temperatures. Therefore, growth at the body temperature of warm-blooded animals is unusual for these fungi. However, some yeasts have adapted to grow at these temperatures and contain some of the most serious fungal pathogens of humans and animals. Their phylogenetic placement in the Dikarya is shown in Fig. 7.2.

7.2.1 Candida and Former Candida Species

The polyphyletic genus Candida comprises some of the most widely studied yeasts with relevance to human health (Daniel et al. 2014). Several species of the genus are part of the mycobiome associated with healthy individuals, and at least Candida albicans is ubiquitous in the human gut. However, people with compromised immune system might suffer from serious health issues (e.g., Fig. 7.1a; Cui et al. 2013; Huffnagle and Noverr 2013; Smeekens et al. 2016). Most indications are associated with dysfunctions of the intestinal tract. As saprotrophic ascomycetous yeasts, Candida spp. grow well in high sugar concentrations, and dietary shifts are the primary advice in such cases. However, severe infections are also reported for almost all organs, including skin, vagina, lung, heart, and brain. Especially, infection via the bloodstream causes severe secondary invasive infections. These represent some of the most serious complications during organ transplantations or HIV infections and are still difficult to treat medically (e.g., Miceli et al. 2011; Clancy and Nguyen 2013; Silveira and Kusne 2013).

Taxonomically, Candida has been a catchall genus for white ascomycetous yeasts that were distinct from Saccharomyces. Although major efforts have been made to resolve the phylogeny and taxonomy in the last decade, it is still a large genus containing several polyphyletic lineages (Daniel et al. 2014). Besides C. albicans, four species (Candida glabrata, Candida parapsilosis, Candida tropicalis, and Candida krusei, the last currently Pichia kudriavzevii) account for 90% of diagnosed cases of invasive candidiasis (but see Clancy and Nguyen 2013). Because proper species identification of the pathogen is still rare, most treatment advices are based rather on the clinical syndrome than on the causative strain or species (Antinori et al. 2016). However, among the possible threats of such symptomatic treatments is missing out on potential multi-resistant species such as Candida auris (e.g., Lockhart et al. 2017).

The clade including C. albicans is currently well circumscribed, but others are still in need of thorough analysis. Multigene phylogenies are needed to resolve the various clades, and often new genera need to be established to provide a taxonomy based on monophyletic lineages (e.g., Kurtzman and Robnett 2014; Shen et al. 2016). However, so far it seems that pathogenicity is restricted to the C. albicans clade and other lineages are not hazardous to humans. Yeasts found in the association with candidiasis in humans are discussed in detail in Chap. 8 of this book.

7.2.2 Cryptococcus

Serious human infections can also be caused by Cryptococcus spp. (Fig. 7.1b), which occur in other mammals, besides humans as well. Although most relevant in the tropics and the Southern Hemisphere, cryptococcosis received only broader attention after an outbreak on Vancouver Island in 1999 (Galanis and MacDougall 2010). The causative agent was identified as a single species, Cryptococcus gattii (currently Cryptococcus bacillisporus). Detailed studies in the last decades however revealed a complex of several species and hybrids to be involved in cryptococcosis in general. In the meanwhile, Cryptococcus neoformans (formerly Filobasidiella neoformans) s.l. is probably the best-studied yeast in terms of its mating system and variation of its life cycle (e.g., Hull and Heitman 2002; Heitman et al. 2011). Due to its importance as human pathogen and model organism, a separate chapter addresses the most recent advances. We therefore refer the reader to Chap. 8 of this book and earlier reviews on the topic (e.g., Idnurm et al. 2005; Lin and Heitman 2006; Heitman et al. 2011). However, it is important to document that species of the Cr. neoformans species complex are not obligate pathogens and human-to-human transmission of the infection is either absent or rare (e.g., Gerstein and Nielsen 2017). Since these yeasts are present in the environment, biotic and abiotic factors are responsible for strain diversity of Cr. neoformans s.l. in terms of physiological properties and virulence traits (e.g., Gerstein and Nielsen 2017).

For a long time, the genus Cryptococcus has been used to accommodate diverse and often distantly related species of Tremellomycetes, which often resulted in confusion between pathogenic and nonpathogenic species. Recent changes in the taxonomy of basidiomycetous yeasts have restricted the genus Cryptococcus to the Filobasidiella clade (see Fonseca et al. 2011). This clade currently comprises seven clinically relevant (Hagen et al. 2015) and two presumably saprobic species, Cryptococcus amylolentus and Cryptococcus depauperatus (Liu et al. 2015). Another species, Cryptococcus luteus (originally Filobasidiella lutea), has been placed in the genus based on the morphological similarity of the sexual stage, but cultures and sequence data for this species are currently missing (see Liu et al. 2015). The two species Cr. depauperatus and Cr. luteus were found as parasites of other fungi, i.e., Lecanicillium lecanii (now Cordyceps confragosa) and Granulobasidium vellereum, respectively. Examples of mycoparasites of this lineage are discussed below in this chapter.

7.2.3 Cutaneous Yeasts

7.2.3.1 Malassezia

The human skin is the most relevant organ besides the intestinal tract in terms of microbes including fungal diversity. Millions of microbial cells inhabit the skin, and most form part of the healthy skin microflora (see Chap. 8 of this book for more details). Although the research on the diversity and function of this microbiome is still in its infancy, several studies highlight the relevance of certain fungal taxa. Malassezia (Malasseziomycetes, Ustilaginomycotina) is a common genus found in many skin microbiome studies (e.g., Findley et al. 2013; Cabañes 2014). Skin colonization by Malassezia species of healthy humans starts at birth, and abundance increases in the first weeks of life. As with other described yeast taxa, only few healthy people suffer from infections caused by Malassezia (see Cabañes 2014). The clinical syndromes are skin discolorations (Fig. 7.1c) and sometimes itchiness, and some species have been related to dandruff. Due to the relative harmlessness, Malassezia has received less attention than to other human pathogens. However, two species, Malassezia furfur and Malassezia pachydermatis, have been reported to cause yeast systemic infections at a low percentage. However, frequency of these infections could be underestimated as not all commonly used culture media contain lipids, which are essential for isolation and detection of these fungi (see below). Mal. pachydermatis is considered to be zoophilic and is frequently found on wild and domestic carnivores. This species is usually associated with otitis externa and different kinds of dermatitis in domestic animals, especially in dogs (see Cabañes 2014). This yeast is occasionally found on the human skin, and its zoonotic transfer from dogs has been documented (see Cabañes 2014).

Biology and evolutionary relationships of these yeasts are highly interesting. It is known as anamorphic yeast only and forms a monophyletic lineage in the Ustilaginomycotina (Begerow et al. 2000; Wang et al. 2015a). No sexual structures could be identified so far, but genome sequencing of this lineage suggests that a sexual state might exist (reviewed in Begerow et al. 2014). All of the known species are bound to warm-blooded animals and especially to respiratory glands. They are lipophilic and require special media for growth. All but one species (Mal. pachydermatis) do not grow in pure culture without external oils added into the medium and are therefore often not detected in culture-dependent surveys. They are, however, detected by analysis of DNA amplicon libraries (e.g., Cabañes 2014; Findley and Grice 2014). Not only isolation but also proper preservation and identification of Malassezia isolates can pose some difficulties.

Malassezia species have been isolated from almost all domestic animals, from different wild animals held in captivity, and also from wildlife (see Cabañes 2014). However, these reports are often fragmentary to provide a good overview on the occurrence of these yeasts on the skin of different animals. In spite of the limited physiological abilities of these yeasts, the detection of Malassezia in environmental samples is of special interest. In a few cases, like in the sequence libraries prepared from deep-seawater samples, Malassezia-related sequences were surprisingly prominent (Bass et al. 2007). Likewise, these yeasts were detected among marine fungal communities associated with corals and sponges (Gao et al. 2008; Amend et al. 2012). Amplified fungal ITS1 fragments subjected to RFLP analysis indicate the presence of Malassezia restricta and Malassezia globosa in soil nematodes (Renker et al. 2003).

7.2.3.2 Trichosporon and Former Trichosporon Species

Dimorphic yeasts producing hyphae breaking into segments (arthroconidia) and lacking sexual stages formerly classified in the phenotypic genus Trichosporon (Trichosporonales, Tremellomycetes, Agaricomycotina) are another group of yeasts commonly reported as a part of the skin mycobiome (e.g., Guého et al. 1994; Mariné et al. 2015). About one third of known former Trichosporon species are correlated with human infections or allergies (Weiss et al. 2014). Trichosporon cutaneum (currently Cutaneotrichosporon cutaneum), Trichosporon inkin, Trichosporon loubieri (Apiotrichum loubieri), and Trichosporon ovoides are the most prominent species involved in superficial trichosporonosis (e.g., white piedra), while Trichosporon asahii, Trichosporon asteroides, and Trichosporon mucoides (Cutaneotrichosporon mucoides) are associated with invasive infections in immunocompromised patients (e.g., Guého et al. 1994; Miceli et al. 2011; Mariné et al. 2015). These yeasts are also frequently mentioned among non-Candida and non-Cryptococcus yeasts in the clinical practice (e.g., Miceli et al. 2011; Chitasombat et al. 2012). For instance, Trichosporon dermatis (Cutaneotrichosporon dermatis) has been shown to be involved in summer-type hypersensitivity pneumonitis (SHP), an allergic disease occurring in hot and humid seasons in Asia that is caused by inhalation of arthroconidia (Sugita 2011). Another species, Tr. asahii, colonizes the gastrointestinal tract of healthy subjects (Cho et al. 2015). The detected genotypes were almost identical to those of reported clinical isolates suggesting that the development of trichosporonosis is probably caused by the normal fungal gut microbiota together with additional unknown factors. However, pathogenicity cannot be unequivocally demonstrated for all former Trichosporon species, as many of them do not grow at 37 °C.

Trichosporon yeasts have been reported from different habitats (e.g., plant material, soils, insects) and geographical regions. The taxonomic heterogeneity of arthroconidia-forming yeasts in the genus Trichosporon has been demonstrated with phylogenetic analyses based on the ribosomal LSU and ITS sequences (Fell et al. 2000; Scorzetti et al. 2002; Middelhoven et al. 2004). As a result, Trichosporon pullulans (currently Tausonia pullulans, Mrakiaceae, Cystofilobasidiales, Tremellomycetes) has been removed from the genus to restrict it to the members of the Trichosporonales (Fell and Scorzetti 2004). As for 2014, the order Trichosporonales comprised several clades (Fell and Scorzetti 2004; Middelhoven et al. 2004; Sugita 2011; Weiss et al. 2014) with dimorphic Trichosporon yeasts and predominantly unicellular Asterotremella, Bullera, and Cryptococcus species (Liu et al. 2015). In spite of the taxonomic complexity, the genus Trichosporon was recently reclassified into six monophyletic lineages (Liu et al. 2015). Clinically relevant species are currently accommodated in the genera Cutaneotrichosporon (Cut. cutaneum, Cut. dermatis, and Cut. mucoides) and Trichosporon (Tr. asahii, Tr. asteroides, Tr. inkin, and Tr. ovoides), whereas most of the saprobic species have been transferred in the reinstated genus Apiotrichum (Liu et al. 2015).

Until the end of the twentieth century, a wide range of species was included under the name of Trichosporon (Pleurococcus) beigelii or synonyms, which were later shown to be phylogenetically distinct (Mariné et al. 2015). The literature lists Cut. cutaneum, Cutaneotrichosporon moniliiforme, and Tr. ovoides as synonyms of Tr. beigelii. It is important to notice that both the name Pl. beigelii and neotypification of Tr. beigelii have been rejected by Guého and colleagues in the beginning of the 1990s (reviewed in Liu et al. 2015). Nevertheless, the name Tr. beigelii is still being reported from clinical samples without a possibility to attribute its detection to any of the recognized yeast species. Both Tr. beigelii and Cut. cutaneum have been reported from environmental samples such as soil, litter, and invertebrates in older studies, which used a limited set of physiological tests for species identification (e.g., Di Menna 1965; Byzov et al. 1993; Carreiro et al. 1997; Sláviková and Vadkertiová 2000). Application of nucleotide sequencing of the ribosomal gene regions identified Apiotrichum porosum and Apiotrichum dulcitum as possible species behind the phenotypic Tr. cutaneum (see for discussion Yurkov et al. 2012; Yurkov 2017). Recently, Trichosporon lactis has been reported colonizing exoskeletons of various dung beetle species of the genus Onthophagus (Górz and Boroń 2016). The yeast grew as unusual epizoic excrescences on the elytra, prothorax, and head of the studied beetles. A few species previously classified in the genus Trichosporon have been isolated from insects, including Scarabaeoidea and identified as Apiotrichum scarabaeorum (Middelhoven et al. 2004). However, yeast proliferation on insect bodies has not been reported before. Whether or not Trichosporon and its relatives are insect pathogens requires additional studies in the future.

7.2.4 Other Important Pathogenic Yeasts on Humans and Animals

The abovementioned species and genera contain probably more than 90% of the described human pathogenic yeasts, but there are many more yeast species known to result in serious infections. Most of them are found frequently in environmental samples and, like many filamentous fungi, seem to be opportunistic pathogens. Disease-causing dimorphic ascomycetes such as Ajellomyces, Histoplasma, Coccidioides, Paracoccidioides, and Blastomyces (Ajellomycetaceae, Onygenales, Pezizomycotina) are known from warm, moist climates and can be found in soils, decaying wood, and bird droppings. The switch from filamentous to yeast growth plays an important role in the infection process, and asexual spores are supposed to be the primary agent. Inability to grow on artificial media hinders our understanding of the infection routes and additionally complicates estimation of the biodiversity of these fungi.

Pneumonia caused by Pneumocystis (Pneumocystidomycetes, Taphrinomycotina) is an important disease of immunocompromised patients. Like the abovementioned ascomycetes, Pneumocystis species cannot be grown in culture, and all stages of the life cycle have to be studied directly in lung tissues. Despite clinical relevance of this dimorphic taxon, profound basic research is lacking. Even diagnostics of many potentially deadly yeast infections are insufficient, and it is currently unknown how many of deathly pneumonias are caused by Pneumocystis, other yeasts, or bacteria as most of them occur in regions with insufficient health care, especially regarding HIV-infections (Thomas and Limper 2007; Skalski et al. 2015).

The asexual ascomycete Macrorhabdus ornithogaster has been isolated from a number of birds, where it infects the stomach. Although this organism was first reported as a yeast in 1980, subsequent studies wrongly named it a “megabacterium” until the identification with DNA sequencing placed this yeast as a member of Saccharomycetales (Tomaszewski et al. 2003). Because cultivation of Mac. ornithogaster was not successful, little is known about its physiological properties and requirements. This yeast however causes widespread infections and occasionally results in devastating disease outbreaks in some bird species (Phalen et al. 2011).

So-called black yeasts represent a heterogenic group in terms of both taxonomy and ecology. Many of these species show pronounced dimorphic growth and are capable of sustaining unfavorable environmental conditions such as desiccation and salinity (e.g., Gostinčar et al. 2010). Members of the genus Exophiala display pathogenicity toward humans and animals (including cold-blooded animals) (e.g., de Hoog et al. 2011; Chowdhary et al. 2014). Clinically relevant species include Exophiala dermatitidis, Exophiala xenobiotica, Exophiala spinifera, and Exophiala oligosperma (Chowdhary et al. 2014). Less common are Exophiala lecanii-corni, Exophiala asiatica, Exophiala phaeomuriformis, Exophiala jeanselmei, Exophiala bergeri, and Exophiala mesophila (Chowdhary et al. 2014). It is important to document that black yeasts can be also isolated from environmental samples (Buzzini et al. 2017; Sannino et al. 2017), as well as in polluted and anthropogenic environments (Novak Babič et al. 2017).

Yeasts have been isolated from various aquatic animals, including clams, mussels, shrimps, isopods, amphipods, crabs, sponges, sea urchins, polychaete worms, fish, and marine mammals (e.g., Hagler and Ahearn 1987; Starmer and Lachance 2011). At least one of them, Metschnikowia bicuspidata, is pathogenic to crustaceans and fish (Lachance 2016). By using its needle-shaped ascospores, the yeast is believed to invade host bodies (reviewed by Lachance 2016). Although some other Metschnikowia species also produce long needle-shaped spores, there is little evidence that species outside the M. bicuspidata clade display parasitic relationships. Lachance (2016) reported the observation of a spore of Metschnikowia hawaiiensis, which is associated with the nitidulid beetle Conotelus obscurus, inside a nematode. The possibility that the nitidulid beetle benefits from the presence of M. hawaiiensis ascospores because the latter might curb infection by parasitic aphelenchoid nematodes was investigated, but could not be confirmed.

Finally, two genera of Ustilaginomycotina, Acaromyces and Meira, have been studied as potential biocontrol agents against citrus mites (Boekhout et al. 2003). Yeasts were found growing on dead insect larvae and endophytically in plant tissues. Their potential parasitism has been hypothesized at the beginning, but further studies showed these yeasts producing glycolipid compounds with a broad inhibition range, which included several fungi pathogenic to plants. The compound has been also shown to have a toxic effect on insect larvae (reviewed in Begerow et al. 2014).

7.3 Plant Parasites

In contrast to animal hosts, plant hosts are much more common among fungal and yeast parasites. Phylogenetic analyses based on genome scale data (Spatafora et al. 2016) support the close interaction between the radiation of fungi and land plants. Although early fungi might have been mutualists of fungi (Redecker et al. 2000), the transition to a parasitic lifestyle is very common and is realized in several lineages. Here we focus on the most relevant yeast lineages in terms of parasitism instead of following a detailed phylogenetic approach analyzing all lineages of Ascomycota and Basidiomycota.

7.3.1 Ascomycota: Taphrina, Protomyces, and Eremothecium

7.3.1.1 Taphrina

The plant pathogenic genus Taphrina is part of the early diverging lineage Taphrinomycotina of Ascomycota (Fig. 7.2), which also includes the fission yeast Schizosaccharomyces pombe, the saprobic yeast Saitoella, the tree-associated Neolecta, the human pathogen Pneumocystis, and the second plant pathogenic genus Protomyces. Most of our present knowledge of Taphrina is derived from the works of Arthur J. Mix, who collected and reviewed older works and provided the first comprehensive list of these fungi (Mix 1949). Verona and Rambelli were the first authors who found the need to provide a formal name (Saprotaphrina) for the asexual states of Taphrina, which they have isolated from flowers and leaf litter (reviewed by Fonseca and Inácio 2011). Because Verona and Rambelli did not provide either a Latin diagnosis of the genus or designated the type species, the genus Saprotaphrina remained invalid, and Moore (1990) proposed the genus Lalaria to accommodate the yeast states of Taphrinales, introducing 23 new species all representing anamorphic forms of previously known Taphrina spp. (Fonseca and Rodrigues 2011). Several Lalaria species have been isolated from the environment, either from healthy plants (see also Kemler et al. 2017) not known as Taphrina hosts or other substrates such as litter and soil (Rodrigues and Fonseca 2003; Fonseca and Inácio 2011). Phylogenetic relationships among the extant authentic Taphrina cultures have been studied using ribosomal gene sequences: the SSU rRNA gene (Sjamsuridzal et al. 1997) and the D1/D2 domains of the LSU rRNA gene and the internal transcribed spacer region (Rodrigues and Fonseca 2003). The existing Taphrina cultures correspond to yeast states that were, in most cases, isolated from infected plant material using the spore-fall method (e.g., Mix 1953). Inácio et al. (2004) discussed the redundancy of the genus Lalaria for the original 23 species proposing to legitimize the use of this genus name only for species isolated in the yeast state where an unequivocal connection to a Taphrina teleomorph could not be established. The number of species accommodated in Lalaria was reduced from 23 to 5 (Fonseca and Inácio 2011), and the subsequent recent changes in the taxonomy of fungi discontinued the practice of using dual names for sexual and asexual morphs, so a few Lalaria species listed by Fonseca and Inácio (2011) have been transferred into the genus Taphrina (Selbmann et al. 2014b). Most Taphrina species and their asexual counterparts display a narrow spectrum of utilized carbon sources, thereby supporting the parasitic lifestyle (Inácio et al. 2004). The species Taphrina inositophila and Taphrina veronaerambellii were frequently isolated from the surfaces of Mediterranean plants not known as Taphrina hosts. They were considered to be true phylloplane yeasts. Interestingly, the two species utilized diverse carbon sources like other phylloplane yeasts. It has been suggested that these two yeasts may have a predominantly saprobic lifestyle unlike other Taphrina species, which are commonly assumed to have a parasitic stage, even if the host and symptoms are not known so far (Moore 1990; Inácio et al. 2004). The genus seems to be distributed worldwide, and even Antarctica harbors at least one species (Selbmann et al. 2014a, b).

The plant pathogenic species in Taphrina cause various symptoms (Fig. 7.1d) on several quite unrelated plant families. While it is best known for the symptoms on Rosaceae, where it causes curly leaves or deformed and aborted fruits like Taphrina deformans on Prunus persica or Prunus dulcis (Cissé et al. 2013), infections of members of other host families result in different symptoms like the witches’ brooms in Fagaceae (mainly Alnus, Populus, and Betula) or just withered leaves in some ferns and/or herbaceous Rosaceae. Infections caused by Taph. deformans and Taphrina betulina are of economic relevance. Most of the studies focused on diseases of economically important fruit trees such as peach, plum, and cherry (Prunus spp.) infected by Taph. deformans. It has been shown that Taph. betulina infection reduces the mean height and diameter of infected Betula pubescens substantially (Spanos and Woodward 1994) and thereby may cause potential losses in timber production within short rotation forestry (McKay 2011).

The unusual ascus formation in and on the plant epidermis is directly followed by a haploid yeast stage, which can reinfect the plant probably after mating. The plant-parasitic hyphal stage of Taphrina is dikaryotic like in members of Basidiomycota, which is not known from other Ascomycota (Kramer 1960).

The genomes of various Taphrina species have been sequenced recently. It encodes a full repertoire of carbohydrate-active enzymes, including those required for degrading plant cell wall components such as cellulose, hemicellulose, and pectin. However, genes for lignin-degrading enzymes are lacking (Cissé et al. 2013; Tsai et al. 2014). Interestingly, the genome encodes targets for known antifungal drugs like azoles, although they are known to be resistant. Thus, additional resistance mechanisms might play a role during the epiphytic stage on leaves (Cissé et al. 2013). In addition, the genome harbors genes putatively involved in the biosynthesis of plant hormones like indole-3-acetic acid (IAA) and cytokinin that might be responsible for the formation of characteristic leaf deformation symptoms (Cissé et al. 2013; Tsai et al. 2014). Another peculiarity of the Taphrina genome is the occurrence of a single copy of the rRNA cistron, which is usually present in several copies in other fungi (Cissé et al. 2013). Environmental sequencing using high-throughput methods revealed members of the Taphrina in analyzed sequence libraries as being among the most frequently observed fungi in some tree leaves (see also Kemler et al. 2017).

7.3.1.2 Protomyces

Reddy and Kramer (1975) reviewed earlier ideas on phylogenetic relationships noting that many other mycologists thought that Protomyces was a “primitive” ascomycete. They also revised morphologically similar fungi (i.e., Burenia, Protomycopsis, Taphrinidium, and Volkartia) and placed them in Protomyceteacea. It is important to document that nucleotide sequences or cultures of other members of Protomyceteacea are lacking and their relationships with the genus Protomyces are thus putative (Kurtzman 2011). Species of the genus Protomyces cause symptoms similar to those caused by Taphrina (Fig. 7.1e). All known Protomyces species are plant parasites causing galls on stems, leaves, and fruits, mainly of Apiaceae and Asteraceae. Similar to Taphrina, members of Protomyces produce a budding yeast-like culture on laboratory media but do not develop hyphae or sexual states unless infecting their host plants (Kurtzman 2011). The yeast colonies are colored in reddish or salmon-like due to the synthesis of carotenoid pigments. Unlike Taphrina, saprobic states of Protomyces are rarely reported from studies, which employed either cultivation or culture-independent approaches. Therefore, our knowledge about asexual yeast states of these plant pathogens is scarce. Substantial economic losses caused by these fungi are rare.

7.3.1.3 Eremothecium

A filamentous member of Saccharomycetaceae, Eremothecium gossypii (syn. Ashbya gossypii), was originally isolated from cotton plant as a pathogen causing stigmatomycosis (Kurtzman and de Hoog 2011). This fungal disease, caused mainly by the two species Er. gossypii and Eremothecium coryli (syn. Nematospora coryli), results in severe economic losses of cotton, coffee, pistachio, and citrus plants in tropical and subtropical areas of the world (Kurtzman and de Hoog 2011). The genus is now comprised by five species, all of which are recognized parasites of plants. Elongated needle-shaped spores of Eremothecium are transmitted to plants by hemipteran insect pests (Kurtzman and de Hoog 2011). Control of the transmitting insects is used to protect crops from stigmatomycosis. Er. gossypii is currently used for industrial production of riboflavin (vitamin B2), which is naturally accumulated by the fungus to protect its spores against ultraviolet light. As the genome has been sequenced, Er. gossypii became also a model to study filamentous growth using the knowledge derived from the first model fungus, Saccharomyces cerevisiae (Wendland and Walther 2005; Perez-Nadales et al. 2014).

7.3.2 Smuts: Ustilago and Other Members of Ustilaginomycotina

Probably the best-studied plant parasites among yeasts are the smut fungi (Fig. 7.1f). The capacity to cultivate them on artificial media is known for more than 100 years and has made them a model system in plant pathological research since then. However, major results and knowledge have often not been incorporated into yeast literature because of unknown links between traditional yeast species and smut fungi and the resulting dual nomenclature of asexual and sexual morphs (Begerow and Kemler 2017). Here, we describe shortly most recent results and the challenges for upcoming yeast research.

Traditionally, only few yeast genera and species have been recognized within the Ustilaginomycotina. Cell wall sugar composition has been used in yeast systematics to characterize yeasts of this subphylum of Basidiomycota. The two major genera Pseudozyma and Tilletiopsis are very vague in their morphological and physiological properties, and a detailed systematic and taxonomic treatment of these yeast taxa was only possible using molecular phylogenetics (Boekhout et al. 1995; Begerow et al. 2000). Since Pseudozyma and Tilletiopsis could not be linked to the genera of their probable teleomorphs, they became catchall genera for yeast strains belonging to Ustilaginomycotina. This resulted in highly polyphyletic assemblages (reviewed in Begerow et al. 2014; Wang et al. 2015a). Although Pseudozyma and Tilletiopsis fulfilled the need formally to distinguish yeast states related to Ustilaginomycetes and Exobasidiomycetes, respectively, these large asexual genera could not accommodate all yeasts in Ustilaginomycotina. As a result, new asexual genera (Farysizyma, Jaminaea, and Sympodiomycopsis) have been described (Sugiyama et al. 1991; Inácio et al. 2008; Sipiczki and Kajdacsi 2009). In the case of Farysizyma, the new genus additionally reduced polyphyly in the yeast genus Rhodotorula (Inácio et al. 2008). As phylogenetic data accumulated, Wang et al. (2015a) consequently proposed to separate monophyletic lineages and either incorporate them directly into teleomorphic genera (or species) or propose new genera for taxa when a direct link to a teleomorph was not known. The teleomorphic genera Sporisorium and Ustilago have been also reclassified and are now restricted to clades with the respective type species (McTaggart et al. 2012, 2016). Out of 20 described Pseudozyma species, 5 could not be assigned unambiguously to any genus and were temporarily (pro temp.) retained as Pseudozyma (Wang et al. 2015a). The biocontrol yeast Pseudozyma flocculosa has been transferred to the genus Anthracocystis (Anthracocystis flocculosa, parasites on Cyperaceae), and the biotechnologically relevant Pseudozyma antarctica has been accommodated in the genus Moesziomyces (Moesziomyces antarcticus, parasites on Poaceae).

Unlike Agaricomycotina, members of the Ustilaginomycotina differ not only in their basidia, fruiting body morphology, and color, but in their ultrastructure as well. The latter resembles the situation within Pucciniomycotina, where several types of septal pores have been established, although the functional relevance of this diversity is unknown (Bauer et al. 1997). Most striking are the differences of cellular interactions with their plant hosts, which are interpreted as driving forces for the adaptive radiation of the whole subphylum Ustilaginomycotina (Bauer et al. 1997; Begerow et al. 2014).

Several studies based on massive isolation of yeasts from the environment have revealed a species diversity, which seems even larger as the current amount of species of smut fungi (e.g., Boekhout et al. 2006). Especially, lineages within inconspicuous plant pathogens like Microstroma or Entyloma could harbor an unknown species diversity. For instance, the recently described species of the genera Jamineae and Sympodiomycopsis in Microstromatales might be just the tip of the iceberg (Wang et al. 2015a; Francesca et al. 2016; Kijpornyongpan and Aime 2017). These yeasts originate from tropical and subtropical regions of the worlds. Their primary habitat is still unknown; however, plant association is likely, as the isolation sources were flowers, wood material, and herbivore insect frass. Boekhout et al. (2006) reported surprisingly high diversity of previously unknown Tilletiopsis species isolated from apple surfaces. Some of these yeasts were phylogenetically placed in the genus Entyloma, but anamorph-teleomorph relationships could not be resolved unequivocally so far. Asexual states of species of Exobasidium (parasitic fungi of Ericaceae) can be obtained in culture by the spore-fall method (Boekhout 1991). Like other anamorphic Ustilaginomycotina, the yeasts belonging to the genus Exobasidium are reported from healthy plants, which are not known as hosts of the parasitic stages (e.g., Inácio 2003). Similarly, yeast states of the grass parasites Farysia were isolated from nonhost plants, flowers, and even fruits (Inácio et al. 2008; Begerow et al. 2014). Recent studies suggest large number of Ustilaginomycotina with saprobic asexual states to be discovered, as exemplified with new genera: Ceraceosorus, Fereydounia, Uleiella, and Violaceomyces (Nasr et al. 2014; Albu et al. 2015; Kijpornyongpan and Aime 2016; Riess et al. 2016). These new fungal lineages were discovered in highly diverse ecosystems, most of which have yet not been intensively explored for their yeast flora.

7.3.3 Anther Smuts: Microbotryum and Allied Fungi

Yeasts in the plant pathogenic lineage Microbotryales (Microbotryomycetes, Pucciniomycotina) have only recently became more prominent in the yeast literature. Only a single species, Rhodotorula hordea (currently Ustilentyloma graminis), was placed in this order. Another yeast from the intestine of a plant bug, Collaria oleosa (Heteroptera, Miridae), collected in Costa Rica was described in the new genus Microbotryozyma (Suh et al. 2012) within the Microbotryales. Unlike other plant parasites, members of Microbotryales are not commonly isolated as epiphytes from plant surfaces (but see Wang et al. 2016). However, they have been isolated from nectar (e.g., Golonka and Vilgalys 2013), and it has been shown that yeasts can proliferate within flowers before infecting (Schäfer et al. 2010). The Microbotryales comprise two families, the Ustilentylomataceae mainly infecting Poaceae and Cyperaceae and Microbotryaceae on dicots including Polygonaceae and Caryophyllaceae (Bauer et al. 2006). So far, it is not clear if all species can be cultivated and include a yeast stage, but at least some members of the genus Microbotryum sporulating in the anthers of Caryophyllaceae (Fig. 7.1g) are easy to cultivate. This made it possible to establish them as a model system for the evolution of host specificity and sexually transmitted disease, as their infection results in male sterile plants (Schäfer et al. 2010). Cultivation success of Microbotryum parasites on Polygonaceae is much lower, and only a few cultures of these species have been reported (e.g., Wang et al. 2015b). Besides the already described yeast Ust. graminis, a potential new Ustilentyloma species has been recently isolated from bean phylloplane (Prior et al. 2017).

While the genus Microbotryum comprises approx. 90 species, the order itself might only include approx. 115 known species in total (Vánky 2012). However, some of the grass-infecting species are very inconspicuous, and there might be a so far overlooked diversity. The phylogeny of Microbotryales is well studied. Dichotomy between monocot- and dicot-infecting lineages has been discussed (Bauer et al. 2006). Within dicot-infecting lineages, radiation on major plant lineages has occurred with an additional specialization to various host tissues (Lutz et al. 2005, 2008; Kemler et al. 2006, 2013; Le Gac et al. 2007; Refregier et al. 2008; Piątek et al. 2011, 2013). Besides being a model system in population genetics, phylogenetics, and infection biology (Schäfer et al. 2010), Microbotryum became also relevant for genomics of plant pathogens. The genome has similar properties as genomes of members in the Ustilaginomycotina, such as amount of genes, paucity of cell wall-degrading enzymes, and a large amount of genes coding for secreted effectors (Kämper et al. 2006; Perlin et al. 2015; Toh et al. 2016), but it also shows some peculiarities (Perlin et al. 2015) which could be related to its different mode of infection (Bauer et al. 1997). The genome comprises, for instance, a large number of genes coding lipases and additionally a repertoire of enzymes that could infer with organ development of the host (Perlin et al. 2015).

7.3.4 Other Basidiomycetes

The dimorphic fungus Itersonilia perplexans (Cystofilobasidiales, Tremellomycetes) causes flower blight in anemone, dahlia, chrysanthemum, and globe artichoke (McGovern et al. 2006). Other symptoms include seedling blight, leaf spots, necrosis, and root cankers in dill, edible burdock, parsnip, and sunflower. Infections caused by It. perplexans resulted in extensive post-harvest losses in cut flower production of China aster and sunflower (reviewed in McGovern et al. 2006). Serious infections by the pathogen were also observed on different herbs including carrot, dill, coriander, parsley, and parsnip in European countries. Growth, sporulation, and infection of It. perplexans are favored by high humidity and cool temperatures. Therefore, post-harvest damage from this fungus may occur in cut flowers held under refrigeration (reviewed in McGovern et al. 2006).

Recently, the yeasts Naganishia adeliensis and Naganishia uzbekistanensis (Filobasidiales, Tremellomycetes, Agaricomycotina) were reported to cause stem and branch canker on stone fruit trees in Iran (Dehghan-Niri et al. 2015; Borhani and Rahimian 2016). These species are known from live and senescent plant material and soils (e.g., Pozo et al. 2011; Yurkov et al. 2015; Mokhtarnejad et al. 2016) and were not previously associated with any disorder of plants.

Kriegeria eriophori (Kriegeriales, Microbotryomycetes, Pucciniomycotina) is phytoparasitic, and the sexual stage develops only on the host plant (Cyperaceae). A few yeasts in genera Meredithblackwellia, Phenoliferia, and Yamadazyma phylogenetically related to Kriegeria were described from plants, soil, and glaciers (e.g., Branda et al. 2010; Wang et al. 2015b). The family Kriegeriaceae is a sister to Camptobasidiaceae, which is comprised by the predominantly psychrophilic yeasts Glaciozyma and putative aquatic mycoparasite Camptobasidium hydrophilum (Toome et al. 2013). Mixia osmundae (Mixiomycetes, Pucciniomycotina) is a rare plant parasite, which is found only on ferns in the genus Osmunda (Nishida et al. 2011). It is currently known from Japan and Taiwan only.

7.4 Mycoparasites

The importance of fungi as parasites of plants and animals is well established. But fungal species in general co-occur together with other fungal species in the same community. It therefore should not come as a surprise that some fungal species have evolved the ability to gain their nutrients completely or in parts from other fungi. Considering its potential ecological and evolutionary importance (e.g., Howe and Suberkropp 1993), the knowledge about fungal-fungal interaction is sparse and mostly limited to potential biocontrol fungi, such as species in the genus Trichoderma (e.g., Harman 2006). By involving direct cell contact, mycoparasitism is going beyond the fairly well-reviewed antagonistic activity of yeasts, which involves killer proteins, glycolipids, and other agents (e.g., pulcherrimine) (Vustin et al. 1990; Golubev 2006; Sipiczki 2006, see also Chap. 9 of this book). Below, we summarize the current knowledge about mycoparasitic interactions involving yeasts and yeast-like fungi.

7.4.1 Diversity and Interactions

Yeasts can be parasites or predators on other fungi (Lachance and Pang 1997; Lachance et al. 2000). Ascomycetous yeasts in the genus Saccharomycopsis and related Candida species have been found to share the ability to form infection pegs that penetrate the wall of various other yeast species as well as some molds (Starmer and Lachance 2011). However, comparison of the response of various predacious species to different nutrient regimes disputed this idea (Lachance et al. 2000). These studies instead indicate that the necrotrophic destruction of prey could be a form of competitive exclusion and not the result of a physiological deficiency in essential nutrients like sulfur, as has been hypothesized earlier (Lachance and Pang 1997).

The number of known and potential mycoparasitic yeasts is larger in Basidiomycota than in Ascomycota (comp. Fig. 7.2). Hosts of the basidiomycetous mycoparasites are either Ascomycota or Basidiomycota, and mycoparasitism on Chytridiomycota or Zygomycetes is unknown (Bauer and Oberwinkler 2008). Phylogenetic correlation between the basidiomycetous mycoparasites and their respective host fungi has not been reported (Bauer and Oberwinkler 2008). Parasitic interactions are associated with the sexual (teleomorphic) stage of the life cycle in the Tremellomycetes (Agaricomycotina), Agaricostilbomycetes (Pucciniomycotina), Microbotryomycetes (Pucciniomycotina), Spiculogloeomycetes (Pucciniomycotina), and Cystobasidiomycetes (Pucciniomycotina), which have been studied as dimorphic heterobasidiomycetes (e.g., Bandoni 1995).

Studies of dimorphic heterobasidiomycetes followed two different directions. The first way, taken by traditional mycologists, relied on mycoparasites sampled in the field, which were investigated in the laboratory, including cultivation (or germination) experiments and research of the interaction modes between the parasite and host. As a result, we know that sexual structures of some mycoparasites (e.g., Tremella, Rhynchogastrema, Trimorphomyces) germinate with yeast states. The second way undertaken by yeast researchers included mating experiments to obtain teleomorphic state on the laboratory media (e.g., Bulleromyces, Curvibasidium, Leucosporidium, and Papiliotrema) and the subsequent description of the relevant morphological characters, such as basidial and hyphal morphology. It turned out that species commonly considered as yeasts form a sexual cycle ex situ and display features previously described as an adaptation to mycoparasitism. We also suggest readers to consider earlier reviews on heterobasidiomycetes and mycoparasites by Bandoni (1987, 1995), Bauer and Oberwinkler (2008), and Weiss et al. (2014).

Basidiomycota exhibit two different types of cellular interaction between parasite and host, namely, parasitism with tremelloid haustoria (or fusion interaction) and parasitism involving colacosomes (Bandoni 1995; Bauer and Oberwinkler 2008). Haustoria, thin hyphae growing in close contact with the host hyphae to draw the nutrients (Fig. 7.1h), have been observed in many Tremellomycetes (Agaricomycotina), including the species Bullera alba (originally Bulleromyces albus), Bulleribasidium oberjochense, Dioszegia antarctica, Cr. neoformans, Holtermanniella mycelialis, Rhynchogastrema coronatum, Sterigmatosporidium polymorphum (Cuniculitrema polymorpha), Syzygospora alba, Syzygospora pallida (Christiansenia pallida), Tetragoniomyces uliginosus, and Tremella sp. (e.g., Metzler et al. 1989; Kirschner et al. 2001; Golubev and Golubev 2003). Haustoria-like hyphae have been also reported for Pucciniomycotina, e.g., Classicula, Cyphobasidium, Cystobasidium, Mycogloea, Naohidea, Occultifur, Spiculogloea, and Zygogloea (Bauer and Oberwinkler 2008). The interaction with tremelloid haustoria involves the fusion of parasite and host cell membranes, inducing direct contact of both partners’ cytoplasm (Bauer and Oberwinkler 2008).

Another type of structures responsible for host-parasite interaction observed in culture are colacosomes (Bauer and Oberwinkler 2008). This organelle is formed at the interface between the parasite and its fungal host (Fig. 7.1i). This mycoparasitic organelle was first described in detail from the interaction of the parasite Colacogloea peniophorae (Microbotryomycetes, Pucciniomycotina) and its host Hyphoderma praetermissum (Bauer and Oberwinkler 1991). Colacosomes develop in the contact area between the parasite and its host and are positioned at the inner surface of the parasite cell outside the cytoplasm but inside the cell wall (Bauer and Oberwinkler 2008). These organelles have so far been only found within the Microbotryomycetes and seem to occur in several, distantly related families within this class, thereby indicating a potential early origin or convergent evolution of this trait within Microbotryomycetes. Yeasts commonly thought to be pure saprobes, i.e., in Leucosporidium, Rhodosporidium (currently Rhodotorula), and Sporidiobolus (currently Sporobolomyces), are also known to contain colacosomes, as well as former Rhodotorula yeasts, which are phylogenetically related to the parasite Col. peniophorae (Sampaio et al. 2003, Bauer and Oberwinkler 2008; Wang et al. 2015b).

7.4.2 Pucciniomycotina

Mycoparasites in this lineage include the genera Agaricostilbum, Atractogloea, Camptobasidium, Chionosphaera, Classicula, Colacogloea, Colacosiphon, Cryptomycocolax, Cyphobasidium, Cystobasidium, Heterogastridium, Mycogloea, Naohidea, Occultifur, Rhodotorula, Spiculogloea, Sporobolomyces, Zygogloea, and some species of Platygloea (reviewed in Bauer and Oberwinkler 2008). Some of these fungi (genera Cyphobasidium and Cystobasidium in Cystobasidiomycetes) are lichenicolous, but the spectrum of lichen-associated taxa is most likely much larger as suggested by recent observations of yet undescribed yeasts in Cystobasidiomycetes in the cortex of lichens collected from different regions of the world (Spribille et al. 2016). Unfortunately, the performed phylogenetic analyses do not allow a solid interpretation of the taxonomic position of these yeasts. The authors indicated lichenicolous parasites of the species Cyphobasidium usneicola and Cyphobasidium hypogymniicola (both formerly classified as belonging to the genus Cystobasidium) as the closest match. However, the genus Cyphobasidium is not monophyletic as demonstrated by Millanes et al. (2016), and its position within Cystobasidiomycetes has not been resolved. The observation of the Cystobasidiomycetes yeasts with lichens showing no parasitic interactions goes in parallel with the detection of Fellomyces-related sequences (originally Tremellales sp. A/B) from necrotic parts of the lichen thalli, without any basidiomata or basidiomyceteous hyphae visible (Lindgren et al. 2015). This data indicates that lichens can be a promising source of a yet unknown basidiomycetous, mycoparasitic, yeast diversity.

7.4.3 Ustilaginomycotina

Several ecological adaptations facilitate the ability of asexual Ustilaginomycotina saprobic stages to grow and survive in their natural habitats. Among them is the ability to sustain low temperature, microaerophilic conditions, and antagonistic activity directed toward bacteria and other fungi. Such a behavior is reported for yeasts previously classified in the genera Pseudozyma and Tilletiopsis (reviewed in Begerow et al. 2014). However, it must be emphasized that most of this behavior does not classify as mycoparasitism in the strict sense and is only included for the sake of completeness. Antagonistic reactions toward other fungi were reported for Anthr. flocculosa, Kalmanozyma fusiformata, Sporisorium graminicola, Golubevia pallescens, Phragmotaenium flavum, and Robbauera albescens (formerly Pseudozyma fusiformata, Pseudozyma graminicola, Tilletiopsis pallescens, Tilletiopsis flava, and Tilletiopsis albescens, respectively) which were reported to secrete glycolipids and modified long-chain fatty acids (reviewed in Begerow et al. 2014). Consequently, some Ustilaginomycotina yeast species might even have evolved a mycoparasitic lifestyle, as has been suggested for Till. pallescens, which was repeatedly isolated from basidiocarps of other fungi (Boekhout 2011). Also, GFP-labeled Anthr. flocculosa observed on plants infected with mildew showed strong association with mildew colonies in laboratory experiments (Neveu et al. 2007). It is however unclear whether Anthracocystis (teleomorph is a grass pathogen) and Golubevia species compete for the resources on infected plants or act as hyperparasites.

7.4.4 Agaricomycotina

In the circumscription of the order Tremellales, Bandoni (1984, 1987) indicated mycoparasitism among other characters common for this group of fungi. This view received additional support with time. As reviewed by Weiss et al. (2014), the mycoparasitic lifestyle is a distinctive feature of the teleomorphic stages for many, if not all, members of the Tremellomycetes. Obvious host specificity and morphological evidence, such as the presence of host hyphae inside fruiting bodies of Tremellomycetes and the presence of tremelloid haustoria, indicate such a lifestyle as ancestral in this lineage. Additional evidence of the presumably parasitic lifestyle of many tremellaceous yeasts comes from phylogenetic studies, which showed yeasts previously classified in the genera Bullera and Cryptococcus intermixed with Tremella species (e.g., Fell et al. 2000; Scorzetti et al. 2002; Millanes et al. 2011; Weiss et al. 2014). The recent analysis of 286 type strains of yeast species and 47 basidiocarp-forming Tremellomycetes supported the previous observation regarding close relationships between yeasts and mycoparasites in Filobasidiales, Holtermannialles, Tremellales, and Trichosporonales (Liu et al. 2015).

In Filobasidiales, yeasts related to Cryptococcus arrabidensis are clustered with the lichenicolous genus Heterocephalacria (former Syzygospora) (Liu et al. 2015). The fungicolous species Syzygospora sorana was transferred into the genus Piskurozyma together with Filobasidium capsuligenum (Piskurozyma sorana and Piskurozyma capsuligena, respectively) and several Cryptococcus species (Liu et al. 2015). In the Tremellales, yeasts were observed in almost every clade containing known and putative mycoparasites, i.e., Bulleribasidium (former Mingxiaea), Dioszegia (Di. antarctica), Carcinomyces (former Bullera), Cryptococcus (Fil. lutea and Filobasidiella depauperata), Papiliotrema (former Auricullibuller, Bullera, and Cryptococcus), Phaeotremella (former Cryptococcus), Pseudotremella (former Cryptococcus), Rhynchogastrema (Bandoniozyma yeasts), Tremella sensu stricto (former Cryptococcus), and Tremella clades I and II (sensu Millanes et al. 2011). Other mycoparasitic genera in the Tremellomycetes [i.e., Fibulobasidium, Sirobasidium, Sterigmatosporidium (former Cuniculitrema), and Trimorphomyces] were already known to produce yeast stages in culture. Although members of the Tremella encephala clade (currently Naematelia encephala) are cultivable, no previously described yeast species have been found in this clade (Liu et al. 2015). Yeast stages are also not yet known for the lichenicolous Tremella clade III (sensu Millanes et al. 2011), which also contains the genus Biatoropsis (Liu et al. 2015; Millanes et al. 2016). Both Holtermannia and its putative asexual counterpart Holtermanniella are known to form tremelloid haustoria. The only known sexual species in Trichosporonales, the fungicolous parasite Tetrag. uliginosus, showed weak relationships to the yeast genus Cryptotrichosporon (Liu et al. 2015).

The study performed by Liu et al. (2015) provides a good overview on the phylogeny of Tremellomycetes. As the study reduced polyphyly in this class and attempted to unify taxonomy of sexual and asexual fungi, it provides an excellent starting point to study the evolution of mycoparasitism in this group of Basidiomycota.

7.5 Concluding Remarks

In the eyes of non-specialists, yeasts are often synonymized with the fermenting ascomycete Saccharomyces. However, a unicellular yeast stage is realized in many fungal lineages, and most of these yeast species do not share the typical saccharolytic (or sometimes copiotrophic, i.e., the preference of nutrient-rich environments) lifestyle. Among the growing number of yeast species studied, we observe an increasing percentage of parasitic species—especially dimorphic species tend to be pathogenic at least in parts of their life cycle.

While some species like Candida or Exophiala are prominent opportunistic (not obligatory) parasites in immunocompromised patients, other yeasts have evolved a parasitic stage and cannot complete their life cycle without it. Thus, it becomes increasingly important and more relevant to understand yeasts as a pluripotent unicellular stage of fungi being highly diverse in terms of nutrition mode and ecology.

While human parasites are well recognized in yeast research, yeasts infecting plants and especially fungi are rarely studied, and our knowledge is very scarce. Herewith, we aimed to summarize some of the current knowledge in this field and to point toward further research directions. We would like also to motivate others to study yeasts with respect to their pathogenic capabilities.