Abstract
Even though yeasts are normal inhabitants of almost any type of aquatic environment, in comparison to other type of substrates, relatively little research has been carried out on the factors affecting their biodiversity and distribution patterns. The distinction of a yeast species as transient or resident element of an aquatic habitat has long been challenging and has been one of the main difficulties in the study of yeast diversity in, for example, continental lakes and rivers. The present chapter will provide an overview of our current knowledge on yeast diversity and ecology in continental freshwater and marine environments; in particular habitats like tropical and temperate rivers and lakes, seawater, and glacial melting water bodies will be reviewed. Water temperature and trophic state are major factors determining the yeast community composition in water bodies, and as they get more extreme due to the increase of stress factors such as cold temperatures, UV radiation, and scarce nutrient availability, the prevalence of basidiomycetous yeast gets more notorious. As a result of the evolutionary adaptation to extreme conditions, certain biotechnologically relevant traits became evident in extremophilic aquatic yeasts such as the production of carotenoid pigments, UV sunscreens, extracellular cold-adapted enzymes, etc.
Access provided by CONRICYT-eBooks. Download chapter PDF
Similar content being viewed by others
Keywords
1.1 Introduction
Yeasts, single-celled and free-floating, occur in water habitats, attached to substrates or within animal hosts (Jones and Slooff 1966; Pore and Sorenson 1990; Libkind et al. 2003; Kurtzman and Fell 2006; Yamaguchi et al. 2009). Yeasts are common inhabitants of aquatic environments and their population density, and species diversity depends on the water type and purity (Hagler and Mendoça-Hagler 1981). The biodiversity and distribution of yeasts have been largely overlooked, partly because of the prevailing ideas among microbiologists about the ubiquity of microorganisms (Reche et al. 2005; Yurkov 2017). As a result, yeasts are poorly documented in most reviews regarding freshwater fungi (e.g., Goh and Hyde 1996; Shearer et al. 2007; Wurzbacher et al. 2010). But it is now recognized that yeasts are among the taxa that deserve urgent research on aspects such as species richness and distribution patterns in most ecosystems (Lachance and Starmer 1998). Freshwater lakes and streams, brackish water, sewage-contaminated water, glacier meltwater, and wastewater have been the source of many basidiomycetous yeasts (Cooke 1976; Pore and Sorenson 1990; de García et al. 2010a, b, 2015; Jones et al. 2014) and made them the prevailing taxonomic group of yeasts in surveys of many aquatic ecosystems (de García et al. 2007; Brandão et al. 2011a, b).
Studies on the geographic distribution of aquatic yeast species are scarce, and most of them are focused on polluted water (Nagahama 2006). Yeast species exclusively associated with aquatic habitats are not numerous. For example, the most common ascomycetous yeast isolated from marine waters is Debaryomyces hansenii, a yeast species considered ubiquitous and isolated from many different environments and regions. Other ubiquitous species frequently observed also in aquatic habitats are Aureobasidium pullulans, Rhodotorula mucilaginosa, and Vishniacozyma victoriae (former Cryptococcus victoriae) (Vaz et al. 2011; Brandão et al. 2011a, b, 2017; Buzzini et al. 2012; de García et al. 2012). Some species are endemic to determined regions: for example, Metschnikowia australis is associated with algae, marine invertebrates, and seawater in Antarctica (Lachance 2011b; Furbino et al. 2014). These observations suggest that geographical patterns and local conditions could influence the ecological distribution of aquatic yeast communities. An overview of geographic distribution patterns of yeasts has been recently published (Yurkov 2017).
Although many of the yeast species collected from water bodies may be truly aquatic species (i.e., autochthonous species), it is also conceivable that some species reached the aquatic environment through runoff from the surrounding watershed (i.e., allochthonous species). For yeasts recovered from aquatic environments, such distinction is always challenging, mainly because of our lack of understanding of factors limiting the distribution of most taxa.
The present chapter will provide an overview of yeast diversity and ecology in continental freshwater (lakes and rivers) and in seawater environments.
1.2 Yeasts in Freshwater of Tropical Rivers and Lakes
1.2.1 General Aspects of Tropical Lakes
There is a high diversity in different aquatic environments in tropical ecosystems. These water bodies can be surrounded by forests with huge species richness, or be situated in altitudinal regions with low plant diversity. In addition, these aquatic environments can be located near cities, resulting in a high anthropogenic influence in their water bodies. Lakes and rivers located in protected areas harbor yeast communities where the species composition reflects inputs from terrestrial sources such as soil and plant debris (Medeiros et al. 2008). These yeasts contribute to the recycling of the plant litter in these environments, through the action of extracellular enzymes, obtaining low weight organic carbon and making them available also to other organisms (Medeiros et al. 2012). According to Hagler and Ahearn (1987), oligotrophic clean lakes usually contain less than 100 yeasts l−1, and mesotrophic lakes and rivers have total yeast counts in the range of 100–500 yeasts l−1, whereas eutrophic aquatic environments usually have more than 103 yeast cells l−1. However, Medeiros et al. (2008) reported counts around 3.5 × 103 yeasts l−1 in a pristine lake of Southeastern Brazil. This result suggests that the yeast populations in clean lake waters could be influenced by the influx of allochthonous organic matter in these environments. The majority of species isolated from tropical lakes and rivers are polytrophic generalists (i.e., species which assimilate a wide range of carbon sources). Nutritionally versatile yeasts are likely to colonize aquatic environments with low nutrient concentrations more efficiently (Rosa et al. 1995). In eutrophic water bodies, yeasts with narrow nutritional profiles may occur in high densities due to utilization of simple carbon sources available in these environments. Species as Pichia kudriavzevii (former Candida krusei = Issatchenkia orientalis), Pichia membranifaciens, Candida glabrata (Nakaseomyces clade), and Hanseniaspora guilliermondii may be prevalent in eutrophic aquatic environments (Medeiros et al. 2008; Brandão et al. 2010). These species assimilate a low number of carbon sources and probably survive and grow in eutrophic aquatic environments using simple sugars as glucose, fructose, and sucrose.
In eutrophic tropical lakes, the total yeast counts have been suggested as an indicator of anthropogenic eutrophication, i.e., organic matter concentration (Hagler et al. 1986; Brandão et al. 2010; Carneiro et al. 2015). The densities of total culturable yeasts also correlate positively with the abundance of Escherichia coli and of total coliform bacteria in several tropical water bodies, suggesting that total culturable yeast counts could be considered indicator of the abundance of these bacteria and, as consequence, of fecal pollution in freshwater habitats (Hagler et al. 1986; Brandão et al. 2010; Medeiros et al. 2012; Stone et al. 2012; Carneiro et al. 2015).
The most limiting nutrients in tropical lakes are nitrogen and phosphorus (Lewis 2000). The availability of these compounds can influence the colonization of these environments by yeasts. Rosa et al. (1990, 1995) reported significant positive correlation between total yeast counts and total dissolved phosphate in a paleo-karstic (i.e., karstified rock or area that has been buried by later sediments) tropical lake in Brazil. The species A. pullulans, Deb. hansenii, Naganishia albida (Cryptococcus albidus), Papiliotrema laurentii, Rhodotorula glutinis, Rh. mucilaginosa, and Cutaneotrichosporon cutaneum occurred in the highest frequencies, and a higher yeast diversity occurred during August and February, corresponding to the end of the isothermal and the beginning of the stratification periods in this tropical lake (Rosa et al. 1995). Morais et al. (1996) reported that the yeast species diversity decreased in the other paleo-karstic tropical lake with depth probably due to the absence of fermentative metabolism of most of the predominant species that could limit their distribution to the highly oxygenated surface waters. A probable correlation could exist between yeast counts and zones of nutrient accumulation determined by the thermal stratification of the water column of the lake. Yeasts are heterotrophic microorganisms that tend to be more prominent in habitats where nutrients are available. According to Morais et al. (1996), the predominance of oxidative polytrophic yeasts and pigmented species suggested that these microorganisms were probably carried from soils and foliar surfaces.
The yeast species richness in lakes and rivers is in general higher in tropical than in temperate and cold environments. This highest species richness could probably be related to the occurrence of dense and diverse surrounding plant communities (Fig. 1.1).
1.2.2 Yeast Communities Associated with Tropical Lakes and Rivers
Several works determined the yeast communities associated with tropical freshwater environments using morphological and physiological tests to identify these microorganisms. Most of these studies were done before the year 2000 (Hagler and Mendonça-Hagler 1981; Hagler et al. 1986; Rosa et al. 1995; Morais et al. 1996), and probably several species were misidentified (or not distinguished), becoming difficult to estimate the species richness in these environments. After the sequencing methodologies utilizing regions of the rRNA gene for identification of yeast species become routine, some works determining yeast species richness and diversity in tropical lakes and rivers were published (Medeiros et al. 2008, 2012; Brandão et al. 2010, 2017; Silva-Bedoya et al. 2014). These papers showed that the yeast communities from tropical lakes are dominated by basidiomycetous yeasts, mainly from the genera Apiotrichum, Hannaella, Moesziomyces, Naganishia, and Papiliotrema, as well as to the former polyphyletic genera Rhodotorula and Sporobolomyces (Medeiros et al. 2008; Brandão et al. 2011b, 2017). Ascomycetous yeasts occur in minor densities and are mainly represented by the genera Aureobasidium, Debaryomyces, Meyerozyma, and Pichia (mainly P. kudriavzevii) and species of the clade Candida albicans/Lodderomyces. Most common yeast species isolated from tropical freshwaters are A. pullulans, Deb. hansenii, P. kudriavzevii, Pa. laurentii, Rh. mucilaginosa, and Sporobolomyces japonicus (Medeiros et al. 2008; Silva-Bedoya et al. 2014; Brandão et al. 2017). These species correspond to around 50% of the total yeast isolates of the freshwater environments studied until now. Other species occur in minor frequencies but are consistently isolated from freshwater bodies, i.e., Hannaella luteola, Hannaella pagnoccae, Meyerozyma guilliermondii, Moesziomyces aphidis, Na. albida, and Rhynchogastrema complexa (Medeiros et al. 2008; Brandão et al. 2010, 2017; Silva-Bedoya et al. 2014). Most of the prevalent yeast species isolated from tropical freshwater are considered ubiquitous because they are not restricted to water but found in different environments and sampling sites. These yeasts are also frequently isolated from phyllosphere of terrestrial plants and soils, and their occurrence in the adjacent lakes and rivers might be the result of runoff from surrounding plants and soil particles. Higher occurrence of basidiomycetous (over ascomycetous) yeasts in these environments could be explained by the metabolic versatility of these yeasts, assimilating on average a broader range of carbon sources and being more tolerant to the variation of the physicochemical properties of these water bodies (Brandão et al. 2011b, 2017).
The presence or absence of some yeast species in tropical water bodies has been related to the anthropogenic impact on these environments. The species Kluyveromyces aestuarii is a marine organism and was observed in very high numbers in mangroves in Rio de Janeiro, so that could be considered an indicator species typical for mangroves; its presence in a specific environmental sample suggests the influence of the mangrove habitat, while its absence in mangroves could be related to a non-fecal pollution or other habitat alterations that modify the natural environment (Araújo and Hagler 2011). For example, C. albicans has been isolated on CHROMagar Candida from tropical lakes and rivers subjected to fecal pollution in Southeastern Brazil (Rosa, unpublished data). This species occurred in counts around 5.0 CFU ml−1 in rivers subjected to fecal pollution, and it was absent in lakes and rivers located in protected ecological reserves. Brandão et al. (2010) studied the yeast occurrence in three lakes of Southeastern Brazil and reported that the yeast densities, determined by the multiple-tube fermentation technique, were significantly correlated only with the density of fecal coliforms. Clinically relevant yeasts, P. kudriavzevii, Mey. guilliermondii, and Candida tropicalis, were the most frequently isolated species in this work and are associated with fecal contamination of water by warm-blooded animals.
Medeiros et al. (2008) and Brandão et al. (2010) tested the yeasts isolated at 37 °C in relation to their susceptibility to commonly used antifungal drugs: ketoconazole, fluconazole, itraconazol, and amphotericin B. These authors verified that several species were resistant to all antifungals tested, and approximately 20% of the isolates were resistant to amphotericin B. Several species isolated from lakes and rivers in Southeastern Brazil showed the virulence factors such as production of proteinases and phospholipases and were able to adhere to human buccal epithelial cells (Rosa, unpublished data). The presence of yeast strains resistant to commonly used antifungal drugs and isolation of strains producing virulence factors suggest that these environments, when affected by fecal pollution, can pose potential health risks for people utilizing these waters for recreation.
Some new species were recently described based on isolates obtained from tropical aquatic environments. For example, Saturnispora serradocipensis was isolated as a minor component of a yeast community from leaf detritus immersed in a tropical stream in the National Park of the Serra do Cipó, Minas Gerais State, Brazil (Canelhas et al. 2011). Rhynchogastrema (originally Bandoniozyma) aquatica was isolated from a freshwater lake surrounded by Atlantic Rain Forest, whereas Rhy. (Bandoniozyma) complexa was isolated in two lakes of the Amazonian region and other substrates, including bromeliad leaves (Valente et al. 2012). Yarrowia porcina was obtained from sediment of a tropical freshwater river in Southeastern Brazil (Nagy et al. 2014). This river was exposed to different types of human influence, namely, cattle farming, mining, and domestic and industrial effluents (Medeiros et al. 2008; Nagy et al. 2014).
1.3 Yeasts in Freshwater of Temperate Lakes and Rivers
1.3.1 Yeast Diversity in Temperate Lakes and Lagoons
Due to a combination of solar heating and wind mixing of surface water layers, most lakes and lagoons in temperate regions are characterized by a fairly predictable seasonal pattern, with alternate cycles of layering and complete mixing. A number of studies investigated the yeast diversity in temperate lakes and lagoons using both culture-dependent and culture-independent approaches. The occurrence of yeasts in lake and lagoon ecosystems is common and is frequently influenced by allochthonous species external sources, including living and decaying plants and animals (Kurtzman and Fell 2004). The complete list of yeast species found in habitats associated with temperate lakes and lagoons is reported in Table 1.1. None of the papers reported the dominance of either Ascomycota or Basidiomycota phyla.
European lakes and lagoons were studied since the early 2000s. Bogusławska-Was and Dabrowski (2001) investigated the yeast diversity in strongly eutrophic waters and bottom sediments sampled in the Szczecin Lagoon, Poland. Yeast abundance in sediments and waters reached maximum in May and July, respectively. A total of 21 species of fungi including yeasts and yeastlike dimorphic fungi were found: most species were shared between both environments, while A. pullulans was only observed in water samples, and Candida inconspicua, Candida utilis (now Cyberlindnera jadinii), and Pichia carsonii (Priceomyces carsonii) were characteristic of bottom sediments only. Candida famata (Deb. hansenii) and Rh. mucilaginosa were the dominant species.
Culture-independent approaches were also used to study yeasts in aquatic samples. A 18S rRNA PCR survey was applied to study the eukaryotic community of the Lake Pavin, France. Of the 16 environmental fungal sequences, two were putatively identified as belonging to the basidiomycetous species Rhodosporidium diobovatum (currently Rhodotorula diobovata) and Filobasidium globisporum and one close to the ascomycetous yeast Taphrina letifera (Lefèvre et al. 2007). More recently, Monchy et al. (2011) studied fungal diversity in lake waters collected along transects from the shore to the center of Lake Pavin and Lake Aydat, France, using a twofold approach, including both cloning/sequencing of the 18S, ITS1, 5.8S, ITS2, and partial 28S region and the pyrosequencing of 18S rRNA hypervariable V2, V3, and V5 regions. Fungi represented about 50% of the total operational taxonomic units (OTUs) identified in Lake Pavin and 30% in Lake Aydat and were dominated by sequences of Chytridiomycota. Pyrosequencing yielded Saccharomycetales as the sole Ascomycota in both lakes, while Basidiomycota sequences were mainly retrieved in the riparian areas of Lake Aydat.
Yeasts and filamentous fungi were collected from a number of stations throughout Lake St. Clair, Canada. The predominant basidiomycetous yeast isolates were identified as Rh. mucilaginosa, Cystobasidium minutum (Rhodotorula minuta), Rh. glutinis, and Sporobolomyces sp. (Kwasniewska 1988). Besides, Ishida et al. (2015) studied eukaryotic diversity of mesotrophic Lake Biwa and eutrophic Lake Inba, Japan. Results revealed that aquatic fungi included not only members of Chytridiomycota but also members of Aphelida, Cryptomycota, and yeasts, in particular the species Deb. hansenii, which was found on the surface of diatom cells from Lake Biwa (Ishida et al. 2015).
1.3.2 Yeast Diversity in Temperate Rivers and Creeks
Although a number of studies have found yeasts in temperate rivers and creeks, the identification of autochthonous populations was sometimes problematic because several yeast species seem to be very versatile, and, therefore, their isolation is not considered sufficient to infer any type of ecological association with aquatic sources. Yeasts represent a regular component of eukaryotic populations in freshwaters of temperate rivers and creeks (Kurtzman and Fell 2004). The complete list of yeast species found in temperate rivers and creeks (and associated habitats) is reported in Table 1.2.
The first studies on yeast diversity in temperate rivers and creeks are dated back to the early 1970s. Simard and Blackwood (1971a, b) found that culturable yeast abundance in water samples collected at St. Lawrence River, Canada, was considerably higher in July and somewhat higher in September. A wide range of ascomycetous and basidiomycetous yeasts was identified with no phylum prevalence. In particular species belonging to the polyphyletic genera Candida and Rhodotorula were the most abundant, and the species Rh. glutinis was the most frequently found (about 58% of the total isolates). However, the taxonomical identity of these isolates should be analyzed with care given that the correct identification of those species is only possible using molecular techniques.
The Danube is the second longest European river and is located in Central and Eastern Europe. Slávikova and Vadkertiová (1997) studied the culturable yeast diversity in water samples of Danube collected in the area of Bratislava. Yeast abundance ranged from 102 to 103 CFU l−1. The species A. pullulans, Candida maltosa, C. krusei (P. kudriavzevii), Geotrichum candidum (Galactomyces candidum), and Saccharomyces cerevisiae among Ascomycota and Cystofilobasidium capitatum and Rh. glutinis among Basidiomycota were the most frequently found. Among them, S. cerevisiae was the dominant species (isolated from 50% of samples and about 25% of isolates). However, it should be kept in mind that the eutrophy of the Danube passing through different cities along the course could have influenced the natural composition of yeast communities.
Some rivers and creeks of the Iberian Peninsula have received particular attention since the 2000s. The Tagus is the longest river on the Iberian Peninsula. It is 1038 km long and spans 716 km in Spain, 47 km along the border between Portugal and Spain, and 275 km in Portugal, where it flows into the Atlantic Ocean. Temperature gradient gel electrophoresis (TGGE), including nested PCR to obtain fungal amplicons containing the D2 domain of the 26S rRNA gene, TGGE band extraction, re-amplification, and sequencing, was used for assessing yeast diversity in the estuary of the Tagus. Fourteen fungal taxa were detected and all except one were yeasts. Most yeast sequences corresponded to members of the Ascomycota and only three belonged to the Basidiomycota. The dominant species were Deb. hansenii, Rh. mucilaginosa, and Cryptococcus longus (currently Vanrija longa) (Gadanho and Sampaio 2004). More recently, de Almeida (2005) found that yeast occurrence in waters sampled at the Tagus estuary did not seem to depend upon tides, but river discharge had a dramatic impact on both the density and diversity of the community. Seasonal changes and yeast abundance were the highest around February/March as the result of the winter peak of the river flow. The main species found were Candida catenulata (currently Diutina catenulata), Candida intermedia, Candida parapsilosis, Clavispora lusitaniae, Deb. hansenii, and Pichia guilliermondii (currently Mey. guilliermondii) among Ascomycota and Rh. mucilaginosa and Rhodosp. diobovatum (currently Rh. diobovata) among Basidiomycota. Interestingly, Coelho et al. (2010) found a correlation between the occurrence of both C. parapsilosis and P. guilliermondii and the incidence of the bacterial fecal species E. coli in waters sampled in Tagus estuary.
Other Iberian rivers have been also taken into consideration. Sampaio et al. (2007) studied the culturable yeast populations occurring on submerged leaves (alder, eucalyptus, and oak) in a natural mountain stream of River Olo, Portugal. Seventy-two yeast taxa were found, and basidiomycetous species predominated over ascomycetous ones. In all leaf litter types, three ubiquitous yeast species, such as Cr. albidus (Na. albida), Deb. hansenii, and Rh. glutinis, were found.
The occurrence and diversity of culturable yeasts in water sampled in River Tinto, which is located in the Iberian Pyrite Belt, a vast geographical area with particular geological features that stretches along much of the south of the Iberian Peninsula, from Portugal to Spain, was studied. In the Iberian Pyrite Belt, acid rock drainage gives rise to aquatic habitats with low pH and high concentrations of heavy metals and causes important environmental peculiarities. Twenty-seven yeast species were detected, 48% of which represented undescribed taxa. A few species, namely, Candida fluviatilis and Rhodosporidium toruloides (currently Rhodotorula toruloides), occurred in situations of intermediate environmental stress (Gadanho et al. 2006). Comparable results were found in a similar environment but in this case of volcanic origin, the River Agrio as described by Russo et al. (2008). Several species/lineages were common to both acidic rivers and showed interesting physiological adaptations to such extreme environments (Gadanho et al. 2006; Russo et al. 2008, 2010, 2016).
1.4 Yeast Diversity in Seawater
1.4.1 General Aspects
The presence of yeasts has been recognized in all worldwide oceans, from coastal regions to offshore environments (including oceanic surface, deep waters, and sediments). Marine fungi including yeasts are known to inhabit a wide variety of habitats within the marine environments (Mouton et al. 2012). The first observation of yeasts in marine water was reported by Fischer and Brebeck (1894). Marine yeasts are believed to have physiological adaptations to overcome the adverse effect of salinity and high hydrostatic pressure and to grow and interact with other microbial marine communities (Lorenz and Molitoris 1997; Kandasamy et al. 2012; Rédou et al. 2015). However, the ecological significance of the presence of viable yeast cells in these habitats as the result of a mere survival under the harsh environmental conditions occurring in seawater environment or, on the contrary, the result of their ability to play an active role in this niche (or even a combination of both) is still an open question (Mouton et al. 2012). Researches on ecology and diversity of marine yeasts have been reviewed in recent years (Kutty and Philip 2008; Nagano et al. 2010; Fell 2012; Kandasamy et al. 2012). The genera and species found in worldwide marine habitats are reported in Table 1.3.
1.4.2 Yeasts in Coastal Marine Environments
Coastal marine waters are subjected to terrestrial influxes due to natural drainage and human activities, and most fungi, including yeasts, can be considered as facultative marine fungi with a presumably terrestrial origin. Terrestrial and human-associated allochthonous yeasts are introduced into these waters by rains and rivers, and their persistence is related to the ability to sustain the saline conditions occurring in seawater. The cell abundance in some cases can be as high as thousands of cells l−1 (Fell 2012). A number of ascomycetous and basidiomycetous yeasts have been found as inhabitant of both terrestrial and nearshore marine environments. The most frequently isolated species were C. parapsilosis, Deb. hansenii, and a few members of the genus Malassezia (Gao et al. 2008; Fell 2012) (Table 1.3). Many of these species were most likely introduced from the surrounding terrestrial vegetation, including mangrove habitats (Statzell-Tallman et al. 2008). The yeast diversity in aquatic ecotone habitats (estuaries, mangroves, salt marshes, bogs, and phytotelmata) is also reported in Chap. 2 of this book.
Some species have been regularly found in coastal marine habitats, namely, Cryptococcus marinus (currently Bandonia marina) and K. aestuarii (van Uden and ZoBell 1962; Fonseca et al. 2011), while a few Metschnikowia species, namely, M. australis, Metschnikowia bicuspidata, and Metschnikowia krissii, are either endemic or restricted to marine nearshore habitats, sometimes associated with marine invertebrates and fishes (Fell and Hunter 1968; Seki and Fulton 1969; Donachie and Zdanowski 1998; Ebert et al. 2000a, b; Moore and Strom 2003; Wang et al. 2008; Lachance 2011b).
Coastal marine sediments represent peculiar environmental niches. Mouton et al. (2012) studied several fungal isolates obtained from marine sediments collected close to St. Helena Bay Western Cape, South Africa. Among them, Rh. mucilaginosa and Yarrowia lipolytica were found. More recently, Hassanshahian et al. (2012) isolated some Y. lipolytica strains from oil-polluted sediment and seawater samples collected in the Persian Gulf (Iran). The strains showed a high ability to degrade aliphatic hydrocarbons.
Several studies also reported the direct pollution of marine nearshore habitats with clinically important yeasts: C. albicans, C. tropicalis, and some Trichosporon spp. strains including Trichosporon asahii were isolated from worldwide bathing beaches (Velegraki-Abel et al. 1987; Papadakis et al. 1997; Vogel et al. 2007; Chen et al. 2009; Sabino et al. 2011) and polluted sediments and shrimps (Hagler et al. 1986; Pagnocca et al. 1989; Soares et al. 1997).
1.4.3 Yeasts in Offshore and Deep-Sea Marine Environments
Due to the high costs involved in offshore sampling, oceanographic studies are limited in number. Although the frequency of occurrence is depending on the source and geographical origin of samples, Kandasamy et al. (2012) reported that the yeast abundance increases with increasing distance from the coastline and increasing depth of coastal sea. Conversely, Fell (2012) reported that in offshore regions there is a reduction in the diversity of species and population densities. Bass et al. (2007) postulated that yeasts are the prevalent form of fungi in the deep sea, as revealed with a culture-independent assay. This hypothesis is consistent with that reported by Fell (2012) who suggested that the unicellular lifestyle is apparently better adapted to the aqueous environment than fungal hyphae. Numerically, yeast cells in open ocean waters ranged from 0 to 10 cells l−1, although regions of high organic activity can result in intensive yeast proliferation (Fell 2012). The yeast genera and species found in worldwide offshore marine water are reported in Table 1.3.
Generally, basidiomycetous yeasts account for the majority of the total yeast population in oligotrophic oceanic water, while the ascomycetous yeasts constitute the majority of the total yeast population in the offshore marine sediments (Kandasamy et al. 2012). For example, a number of basidiomycetous yeasts were isolated in seawater collected in the Atlantic Ocean (southern Portugal). Specifically, Rhodosporidium babjevae, Rhodosp. diobovatum (currently Rhodotorula babjevae and Rh. diobovata, respectively), and Pseudozyma aphidis (currently Moesz. aphidis) were the most frequently found species (Gadanho et al. 2003). Among the ascomycetes, some Candida species and Deb. hansenii were found as inhabitant of offshore and deep-sea oceanic habitats (Kandasamy et al. 2012), in agreement with the early study of Hagler and Ahearn (1987), who postulated that Deb. hansenii can be considered the most common ascomycete in marine waters.
Although they have been occasionally isolated from nonmarine sources, some species were found to inhabit specific water masses or oceanographic regions. Among them, Blastobotrys parvus (formerly Sympodiomyces parvus) was found in warmed Antarctic and sub-Antarctic waters (Fell and Statzell-Tallman 1971), Candida natalensis was isolated in the Indo-Pacific ocean (Fell 2012), and Candida norvegica was found in a narrow geographical area southward from the polar front (Fell 2012). Strains of the species Leucosporidium antarcticum (currently Glaciozyma antarctica) have been isolated in Antarctic waters adjacent to the ice pack (Fell 2012). The yeast diversity in cold Polar, sub-Polar, and non-Polar habitats is also reviewed in Chaps. 11 and 12 of this book.
Nagano et al. (2010) investigated deep-sea sediments (1200–10,000 m) collected off the coast of Japan by a culture-independent approach. A number of unknown species together with OTUs (operational taxonomic units) close to C. parapsilosis, Cryptococcus skinneri (currently Phaeotremella skinneri), Metschnikowia colocasiae, Metschnikowia continentalis, and Metschnikowia kamakouana were found. Singh et al. (2012a) investigated fungal diversity in two deep-sea (5000 m) sediment cores collected in the Central Indian Basin by both culture-dependent and culture-independent approaches. A total of 19 culturable fungi including yeasts and 46 OTUs were found. The most represented yeast species were Deb. hansenii, Rhodotorula slooffiae (currently Cystobasidium slooffiae), Rh. mucilaginosa, and the black yeast Hortaea sp. The detection of amplicon sequences belonging to Exobasidiomycetes and Cystobasidiomycetes from deep-sea samples was also reported (Singh et al. 2012b). Zhang et al. (2014) studied yeast diversity of deep-sea sediment samples collected in the East Indian Ocean. OTUs were related to some yeast species, namely, Candida etchellsii, C. inconspicua, Candida sake, Candida xylopsoci, Dipodascus australiensis, and Gal. candidum among Ascomycota and Cryptococcus curvatus, Cryptococcus fragicola, Cryptococcus podzolicus (currently Cutaneotrichosporon curvatus, Vanrija fragicola, and Saitozyma podzolica, respectively), Guehomyces pullulans (Tausonia pullulans), Cyst. slooffiae, Sporobolomyces lactosus, Sterigmatomyces halophilus, and Trichosporon moniliiforme (currently Cutaneotrichosporon moniliiforme) among Basidiomycota and the black yeast Hortaea werneckii. A recent study on fungi and yeast diversity in the deep-sea biosphere (water depth ranging from about 5000 to 7000 m) of the Pacific Ocean also reported that the 38.5% of environmental sequences were closely related to phylogenetic lineages comprised by yeasts, namely, to the genera Candida, Erythrobasidium, Meyerozyma, Tilletiopsis, Rhodotorula, and unspecified members of the former polyphyletic genera Cryptococcus and Rhodotorula. Several OTUs were also classified as species of the genera Malassezia, Trichosporon (Cutaneotrichosporon), and Sterigmatomyces, which are well-known pathogens or parasites of marine animals (Zhang et al. 2014; Xu et al. 2016). Yeasts as parasites of animals, plants, and other fungi have been recently reviewed (Begerow et al. 2017).
Hydrothermal vents are fissures in a planet’s surface from which geothermally heated water issues. Their presence strongly affects chemistry and biology of the adjacent habitats. The yeast diversity found in marine hydrothermal vents is reported in Table 1.3. Gadanho and Sampaio (2005) explored the culturable yeast diversity in thermal systems of the Mid-Atlantic Ridge. Species identifications reported both marine- and terrestrially associated species. Unknown species represented 33% of the total yeast taxa. The authors reported some species frequently found in marine waters, namely, Candida atlantica, Candida atmosphaerica, C. parapsilosis, Rh. diobovata, and Rhodosporidium sphaerocarpum (currently Rhodotorula sphaerocarpa). Similar results were obtained by Burgaud et al. (2010) from a series of studies at vents in the Mid-Atlantic Ridge, South Pacific Basins, and East Pacific Rise (Table 1.3). On the contrary, Le Calvez et al. (2009) observed the predominant presence of unknown fungal groups, including species of the former polyphyletic genera Cryptococcus and Filobasidium in vents of the Pacific and Atlantic Oceans.
Jin et al. (2014) studied fungal diversity in two South China Sea sponges (Theonella swinhoei and Xestospongia testudinaria) which resulted in 26 OTUs that were assigned to Ascomycota, Basidiomycota, and Blastocladiomycota, including a taxon closely related to the yeast species Cryptococcus gastricus (currently Goffeauzyma gastrica). The fungal composition of both sponges was significantly different from that of seawater.
A few new species inhabiting different offshore marine habitats were recently described. For example, Yarrowia keelungensis was isolated from the sea-surface micro-layer off the northern coast of Taiwan (Chang et al. 2013), while Yamadazyma barbieri was isolated from Mid-Atlantic Ridge ocean water samples located in the direct vicinity of black smokers near the Rainbow deep-sea hydrothermal vent and one from Brazilian marine water samples off the Ipanema beach (Burgaud et al. 2016). Also, Yam. barbieri is phylogenetically related to a few species of the Yamadazyma clade, which were isolated from marine habitats including deep-sea hydrothermal vents, i.e., C. atmosphaerica, C. atlantica, Candida oceani, Candida spencermartinsiae, and Candida taylorii. These species are widespread in marine habitats and represent an ecologically and phylogenetically defined cluster of marine species in the Yamadazyma clade (Burgaud et al. 2016).
1.5 Glacially Originated Water Bodies
1.5.1 General Aspects
Glacial ice is the largest reservoir of freshwater on Earth and many glaciers, because seasonal climates store water as ice during the colder seasons and release it later in the form of meltwater when warmer summer temperatures occur. As glaciers retreats, many water bodies (lakes, ponds, etc.) are left behind and retain direct connection to the glacier through rivers or streams. Even though most glacial ice is located in the polar regions, continental glaciers may be also found in mountain ranges between 35°N and 35°S like the Himalayas, Andes, Rocky Mountains, and in a few other high mountains, being Greenland and Patagonia the biggest expanses of continental glaciers. When a glacier erodes the land, and then melts, it fills the hole or space that it has created originating glacial lakes. In tropical areas, glacial meltwater is an important water resource for major cities (Cook et al. 2016). As glaciers retreat, which is a global tendency, ice-marginal lakes (or proglacial lakes) become distant water bodies which in most cases remain connected by rivers and streams. Most glacial lakes are in elevated locations and this increases in lower latitudes. Normally they are in remote or even protected areas, with little human influences, such as local pollution or land use change, and can be considerate open systems with surface in- and outflow. Most of these aquatic environments considered oligotrophic are characterized by the presence of very low nutrient levels and low rates of external supply.
1.5.2 Yeast Diversity and Ecology in Patagonian Glacial Water Bodies
An interesting example of oligotrophic water bodies is lakes and rivers of Andean Patagonia in South America. Patagonia, the southernmost region of the United States, extends approximately from 40°S—where the width of the continent is about 1000 km—and gradually narrows southward until it disappears in Cape Horn at 56°S (Coronato 2016). These lakes are mostly of glacial origin, reaching in the case of lakes, depths frequently greater than 100 m. They are extremely transparent due to their oligotrophic or even ultra-oligotrophic condition and have an extended euphotic zone (i.e., layer of seawater that receives enough sunlight for photosynthesis to occur) of about 50 m (Modenutti et al. 1998). Quirós and Drago (1985) classified Andean lakes as warm monomictic with a period of summer stratification. Their characteristic low nutrient concentrations is a consequence of the low chemical weathering of the dominant igneous bedrock, as well as low rates of atmospheric deposition. It has been reported that the presence of marine cyclic cations, dissolved inorganic nitrogen, is much lower than the world average (Pedrozo et al. 1993). Microorganisms thriving in such glacial-originated water bodies are typically exposed to multiple stress factors, namely, low temperatures, lack of nutrients, and increased UV exposure as a result of high elevation and transparency.
An additional description of South American cold habitats and a comprehensive list of psychrophilic and psychrotolerant yeast species recovered from such environments are given in Chap. 12 of this book. In this paragraph, we will focus on specific interesting cases illustrating diversity and ecology of yeasts in the northern Andean Patagonia (Argentina) where a great variety of glacially formed water bodies exist. They are characterized by ultra-oligotrophic to mesotrophic conditions and range from small to large lakes, including small high elevation lakes, sometimes surrounded by dense forest (Quirós and Drago 1985; Díaz et al. 2000) (Fig. 1.1). These habitats are normally exposed to extended daylight (at latitude 41–42°S) and consequently increased UV radiation, due also to ozone layer depletion and a clean atmosphere. As already mentioned, these aquatic environments are highly transparent due to their ultra-oligotrophic character and, thus, substantially affected by UV radiation (Villafañe et al. 2001). It is expected then that yeasts autochthonous to these habitats should display cold tolerance and nutritional plasticity and possess efficient strategies for photoprotection. Thus, although yeasts are ubiquitous components of these aquatic environments, they are often present at much lower concentrations than can be expected in terrestrial habitats, such as soils (103–104 cells g−1) (Spencer and Spencer 1997; Slávikova and Vadkertiova 2000) and phylloplane [102–104 cells (cm2)−1] (Last and Price 1969; Inácio et al. 2002). Yeasts inhabiting soils and phylloplane are reviewed in Chaps. 3, 4, 6, and 7 of this book.
Even though a portion of the yeast species present in a water body might be native to the aquatic system, it is known that a significant proportion of the yeasts present in a water sample had reached the aquatic environment through runoff from the surrounding watershed (Hagler and Ahearn 1987). If this is entirely true, and assuming the absence of microbial growth in the water column, a few hypotheses can be drawn for the yeast cell dynamics in the water column of ultra-oligotrophic and pristine lakes like those discussed here. First, a higher number of yeast cells might be expected in coastal areas than in open waters (pelagic sites) due to dilution effect and higher availability of the organic matter. Second, allochthonous species can be expected to be more abundant in small lakes having a low lake-area-watershed-area ratio, as well as in the littoral (as opposite to pelagic) areas of larger lakes. One can speculate that the proportion of these allochthonous yeasts should be higher in coastal waters, as well as in small lakes having a low lake-area-watershed-area ratio. In contrast, the proportion of autochthonous species must be higher in the pelagic zone of large lakes given they are better adapted to the harsh conditions and can prevail. Finally, if photoprotective compounds (i.e., carotenoids and mycosporines, MYCs) provide adaptation advantages in the pelagic zone of a highly UV-exposed region, then differences in the proportion of species producing either carotenoids or MYCs between these two types of habitats can also be expected.
During studies of several water bodies in Northwestern Patagonia, including lakes, rivers, and ponds, yeasts were found in almost all samples (Libkind et al. 2003, 2009a; Brandão et al. 2011a, 2017), and they normally presented average abundances around 220 ± 389 CFU l−1. Average yeast abundances ranged from 2 to 250 CFU l−1, rarely exceeding 200 CFU l−1, and these numbers are consistent with those reported for other clear lakes (Hagler and Ahearn 1987). A few exception were found in the high-altitude lake Laguna Negra (890 CFU l−1, 93% of red yeasts) and in a few samples from an anthropogenically impacted coast (1668 CFU l−1). The former case cannot be attributed to a high anthropogenic influence because of the secluded location of this lake, but given 87.5% of the pigmented yeasts were Rh. mucilaginosa, it is conceivable that an occasional surge of organic matter caused a temporary increase of this red yeast population (Libkind et al. 2009a) and the carotenoid pigments probably provided this yeast photoprotection (Moliné et al. 2010). In fact, a strain of Rh. mucilaginosa from a high-altitude lake was found as a good carotenoid producer for applied purposes (Libkind et al. 2004a). The latter case (coastal water) showed yeast counts characteristic of eutrophic waters (Simard and Blackwood 1971a, b; Meyers et al. 1970; Hagler and Ahearn 1987) and might indicate an increased availability of organic matter due to the coastal condition (higher availability of vegetal and animal residues). Though in a minor scale, a higher level of viable yeasts was found in anthropogenically affected coastal sites located at San Carlos Bariloche City, coast in the Nahuel Huapi Lake. These sites had higher yeast values (97–141 CFU l−1) than other ones far off the influence of the city (22–73 CFU l−1). Even though further studies should be performed in order to confirm this observation, for oligotrophic lakes such as those from Andean Patagonia, it seems that the total number of yeasts in the water sample serve as a good indicator of anthropogenic impact, given that normally unpolluted waters have very low numbers of yeasts. All other Andean lakes surveyed showed yeast values typical for open waters of non-polluted lakes (Hagler and Ahearn 1987; Nagahama 2006). In a yet unpublished work, 20 water bodies were pooled into two groups depending on whether they were coastal (8) or pelagic sites (12) (Libkind et al. unpublished data). The former group showed higher yeast numbers (442 ± 558 CFU l−1) than the latter group (71 ± 62 CFU l−1). Other studies reported also that open waters of clear lakes yield generally yeast counts below 100 CFU l−1 (van Uden and Ahearn 1963; Meyers et al. 1970; Hagler and Ahearn 1987) and that this value increases with the proximity to the coast (Hagler and Ahearn 1987).
Basidiomycetous yeasts are the predominant group in these type of aquatic cold environments (Libkind et al. 2003, 2005b, 2009b, 2010; de García et al. 2007, 2012; Brandão et al. 2011a). This is similar to other cold habitats and an exhaustive overview of the biodiversity of cold-adapted yeasts (see Chap. 12 of this book). A few authors have suggested that this could be due to a higher nutritional versatility and a higher tolerance to extreme environmental conditions of the basidiomycetous compared to ascomycetous yeasts (Sampaio 2004; Frisvad 2008). As already stated above, UV radiation is a major environmental factor in clear lakes and even more pronounced in Patagonian lakes. Thus, we compared the UV susceptibility of a large representative set of ascomycetous and basidiomycetous yeasts using different culture media (Moliné 2004). Even though results were greatly influenced by the nutritional level of the media, in general ascomycetous yeasts were significantly less tolerant to any of the radiation treatments used in the experiment (PAR, PAR + UVA, and PAR + UVB). This study also suggested that the carotenoid-accumulating yeasts (often referred to as red yeasts) were generally more tolerant than nonpigmented species. Later, using naturally occurring albino strains of Sporobolomyces ruberrimus and Cystofil. capitatum (two species typically found in glacially originated water bodies in Patagonia), Moliné et al. (2009) demonstrated that carotenoid pigments provide protection against UVB. Further experimental evidence of the utility of carotenoids as photoprotectants arose from studies performed with one of the prevailing yeasts in aquatic environments of glacial origin: the ubiquitous red yeast Rh. mucilaginosa (Moliné et al. 2010). In this work, the accumulation of carotenoids, in particular torularhodin, was demonstrated to contribute substantially to enhance UVB tolerance in yeasts. The protective mechanism was shown to be indirect, probably by quenching reactive oxygen species (ROS) as a result of the antioxidant properties of carotenoid pigments. The ability of certain yeast species to synthesize mycosporines, compounds able to directly protect cells from UV radiation (natural sunscreens), was discovered for the first time studying glacially formed aquatic environments (Libkind et al. 2004b, 2006). Mycosporines are water-soluble compounds composed of a cyclohexenone attached to an amino acid (or amino alcohol). Fungal mycosporines absorb light in the UV spectrum with a maximum at 310 nm wavelength (UVB). The primary role assigned to mycosporines was to act as photoprotective UV filters (Shick and Dunlap 2002; Torres et al. 2004), although other roles were also attributed including antioxidant activity, osmoregulation, resistance to thermal stress, and to serve as intracellular nitrogen storage (Oren and Gunde-Cimerman 2007). Most basidiomycetous yeasts isolated from Patagonian lakes were found to synthesize a UV-absorbing compound when grown under photosynthetically active radiation (Libkind et al. 2004b), and this occurred more frequently in species of the subphylum Pucciniomycotina (Libkind et al. 2011b) and Agaricomycotina (Libkind et al. 2005a, 2011c). The main mycosporine found in yeast so far is mycosporine-glutaminol-glucoside (MGG) (Sommaruga et al. 2004) for which the UVB photoprotective role was recently experimentally demonstrated (Moliné 2010; Moliné et al. 2011). Biochemical characterization of yeast MGG further revealed that possesses high photostability and antioxidant properties (Moliné et al. 2011) and thus showing its value as natural UV protectants and as biotechnological relevant compound (Colabella et al. 2014; Libkind et al. 2016).
The occurrence of MGG-positive yeast in glacially originated water bodies goes through a wide range, from 14% to near 90% of total cultivable yeast community (Libkind et al. 2006, 2009a; Brandão et al. 2011a). MGG synthesis was more frequent in yeasts that were not able to accumulate carotenoid pigments such as Cr. albidus (currently Na. albida), Cryptococcus antarcticus (Naganishia antarctica), Cryptococcus saitoi (Naganishia globosa), Cryptococcus festucosus (Holtermanniella festucosa), Cryptococcus adeliensis (Naganishia adeliensis), Cryptococcus magnus (Filobasidium magnum), Gu. pullulans (Ta. pullulans), and A. pullulans (Libkind et al. 2009a; Brandão et al. 2011a), and red yeasts capable to produce MGG were Cyst. minutum (Rh. minuta), Cystobasidium laryngis (Rhodotorula laryngis), and Dioszegia spp. Like for red yeasts, the proportion of mycosporine-positive species was higher for lakes with higher transparency or in pelagic zones (Brandão et al. 2011a). In glaciers meltwater and ice, yeasts, which are able to synthesize MGG, are less frequent and include species like Dioszegia crocea and Dioszegia fristingensis as the most important ones (de García et al. 2012). Dioszegia species were proven to be considerably higher resistant to UVB damage than most other aquatic yeasts (Moliné 2004; Libkind et al. 2009a), probably as a result of its particular carotenoid composition (plectaniaxanthin) (Madhour et al. 2005) and the high levels of MGG they accumulate (Libkind et al. 2005a, 2009a), both explaining their ability to thrive and prevail in extreme environments like those described in this paragraph.
A few studies reported yeasts biodiversity indices (e.g., Shannon-Weaver index; see also Yurkov and Pozo (2017)) of aquatic biotopes in Patagonia and showed that the yeast diversity in these environments (expressed as Shannon diversity index values) seems comparable or even higher than the ones of some in Patagonian forest soils or from tropical lakes (Brandão et al. 2011a, 2017; Mestre et al. 2011; de García et al. 2012). Yeast biodiversity in Patagonian aquatic environments comprises a large number of species. Among carotenoid-producing yeasts, the ubiquitous species Rh. mucilaginosa was the most frequent and commonly found species (Libkind et al. 2003, 2008). Species of the genera Cystofilobasidium, Dioszegia, Rhodosporidiobolus, Rhodotorula, Sporidiobolus, and Sporobolomyces were also isolated, though less frequently. Interestingly, ballistospore-producing yeasts (a characteristic typical for yeasts living on leaf surfaces) were more frequent in aquatic environments under relatively low human impact and in lakes surrounded with dense forest (Libkind et al. 2003). Nonpigmented yeasts were studied in a less extent, but species belonging to the genera Candida and Torulaspora, as well as to the former polyphyletic genus Cryptococcus, were found (Brizzio and van Broock 1998). Other genera like Cutaneotrichosporon, Debaryomyces, Hanseniaspora, Leucosporidium, and Pichia may also occur in waters (de García et al. 2007; Libkind et al. 2009a; Brandão et al. 2011a, 2017). The majority of these species have been already reported to be present in other aquatic environments; however, several novel species of the genera Sporobolomyces and Cystofilobasidium have been described (for recent review, see Buzzini et al. 2012; de García et al. 2014). Recently, Cystobasidium psychroaquaticum was described from psychrophilic aquatic habitats, including oligotrophic lakes and swamps, although a few strains were also found in terrestrial habitats (Yurkov et al. 2015). To be specially mentioned is the finding in coastal areas of glacially formed water bodies of a few isolates of biotechnologically relevant yeasts such as Saccharomyces eubayanus (brewing) and Phaffia rhodozyma (astaxanthin) (Libkind et al. 2007; Brandão et al. 2011a), although these yeasts relevant to the beer and aquaculture industries, respectively, are clearly related to forest substrates rather than water and thus represent an allochthonous species in aquatic environments (Libkind et al. 2011a, d).
1.6 Concluding Remarks
Most yeasts recovered from water samples are actually associated with plants and soils and arrive to the aquatic ecosystems through runoff phenomena, rather than being true aquatic yeasts. This is why quantitative analysis of aquatic yeast communities is complicated due to large variability of data and a large fraction of presumably transient microbiota. The proportion of allochthonous yeasts is influenced by the trophic state of the lake, the surrounding vegetation, water body size, and the number and type of effluents, among other factors. Despite these complications, various interesting niches are present in aquatic environments, especially in marine environments, that deserve special attention due to its fundamental relevance or to the lack of available knowledge. For example, yeasts associated to deep sea (i.e., hydrothermal vents) have been mostly overlooked, and the few studies performed revealed promising results (Gadanho and Sampaio 2005). Macroalgae-associated yeasts are also an interesting topic of research given that species like M. australis show a strong association with this substrate in Antarctica (Godinho et al. 2013). The potential ecoclade (Gadanho and Sampaio 2009) of the genus Yamadazyma is also interesting given these yeast species are mostly found in seawater (Burgaud et al. 2016), and there is evidence that they might be metabolically active, participating in the carbon cycle in these ecosystems.
The application of culture-independent strategies (metagenomics) will allow to have a more clear picture of yeast diversity in aquatic environments. The low number of yeast cells found in many aquatic habitats (10–100 CFU l−1), mostly oligotrophic or ultra-oligotrophic, complicates the use of metagenomic approaches and the achievement of a comprehensive picture of the yeast community. However, these might still be useful for the detection of novel taxa and the relative quantification of the main species of yeasts.
Yeasts inhabiting aquatic environments can be very often subjected to multiple stress factors such as cold temperatures, UV radiation, ultra-oligotrophicity, salinity, etc. Species adapted to one or several of these factors have naturally developed mechanisms to reduce the negative effects of the harsh environmental conditions. Metabolic and physiological characterization of isolated yeasts represents a valuable tool for the identification of potentially autochthonous species and the detection of biotechnologically relevant traits such as the production of carotenoid pigments, UV sunscreens, extracellular cold-adapted enzymes, etc. In the present chapter, we have shown that aquatic environments can act as reservoir of many yeast species bearing physiological adaptations interesting from both fundamental and applied perspectives and that many additional yeast diversity studies are needed in order to increase our incipient knowledge on the factors affecting yeast distribution and composition in water habitats.
References
Abe F, Miura T, Nagahama T, Inoue A, Usami R, Horikoshi K (2001) Isolation of a highly copper-tolerant yeast, Cryptococcus sp., from the Japan Trench and the induction of superoxide dismutase activity by Cu2+. Biotechnol Lett 23:2027–2034
Abe F, Minegishi H, Miura T, Nagahama T, Usami R, Horikoshi K (2006) Characterization of cold- and high-pressure-active polygalacturonases from a deep-sea yeast, Cryptococcus liquefaciens strain N6. Biosci Biotechnol Biochem 70:296–299
Ahearn DG, Roth FJ, Meyers SP (1968) Ecology and characterization of yeasts from aquatic regions of South Florida. Mar Biol 1(4):291–308
Araújo FV, Hagler AN (2011) Kluyveromyces aestuarii, a potential environmental quality indicator yeast for mangroves in the state of Rio de Janeiro, Brazil. Braz J Microbiol 42:954–958
Babu DT, Antony SP, Joseph SP, Bright AR, Philip R (2013) Marine yeast Candida aquaetextoris S527 as a potential immunostimulant in black tiger shrimp Penaeus monodon. J Invertebr Pathol 112:243–252
Bass D, Howe A, Brown N, Barton H, Demidova M, Michelle H, Li L, Sanders H, Watkinson SC, Willcock S, Richards TA (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc Biol Sci 274:3069–3077
Begerow D, Kemler M, Feige A, Yurkov AM (2017) Parasitism in Yeasts. In: Buzzini P, Lachance MA, Yurkov AM (eds) Yeasts in natural ecosystems: ecology. Springer, Heidelberg, pp 179–210
Bogusławska-Was E, Dabrowski W (2001) The seasonal variability of yeasts and yeast-like organisms in water and bottom sediment of the Szczecin Lagoon. Int J Hyg Environ Health 203:451–458
Brandão LR, Medeiros AO, Duarte MC, Barbosa AC, Rosa CA (2010) Diversity and antifungal susceptibility of yeasts isolated by multiple-tube fermentation from three freshwater lakes in Brazil. J Water Health 8:279–289
Brandão LR, Libkind D, Vaz ABM, Espírito Santo L, Moliné M, de García V, van Broock M, Rosa CA (2011a) Yeasts from an oligotrophic lake in Patagonia (Argentina): diversity, distribution and synthesis of photo-protective compounds and extracellular enzymes. FEMS Microbiol Ecol 76:1–13
Brandão LR, Rosa CA, Medeiros AO (2011b) Yeast diversity in freshwater ecosystems. In: Daniels JA (ed) Advances in environmental research. Science Publisher, Hauppauge, pp 207–222
Brandão LR, Vaz AB, Espírito Santo LC, Pimenta RS, Morais PB, Libkind D, Rosa LH, Rosa CA (2017) Diversity and biogeography patterns of yeast communities from lakes of Antarctica, Argentinean Patagonia, and tropical Brazil. Fungal Ecol 28:33–43
Brizzio S, van Broock M (1998) Characterization of wild yeast killer from Nahuel Huapi National Park (Patagonia, Argentina). Food Technol Biotechnol 4:273–278
Burgaud G, Arzur D, Durand L, Cambon-Bonavita MA, Barbier G (2010) Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microbiol Ecol 73:121–133
Burgaud G, Arzur D, Sampaio JP, Barbier G (2011) Candida oceani sp. nov., a novel yeast isolated from a Mid-Atlantic Ridge hydrothermal vent (-2300 meters). Antonie van Leeuwenhoek 100:75–82
Burgaud G, Coton M, Jacques N, Debaets S, Maciel NO, Rosa CA, Gadanho M, Sampaio JP, Casaregola S (2016) Yamadazyma barbieri f.a. sp. nov., an ascomycetous anamorphic yeast isolated from a Mid-Atlantic Ridge hydrothermal site (−2300 m) and marine coastal waters. Int J Syst Evol Microbiol 66:3600–3606
Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241
Canelhas MR, Barbosa AC, Medeiros AO, Lee CF, Huang LY, Lachance MA, Rosa CA (2011) Saturnispora serradocipensis sp. nov. and Saturnispora gosingensis sp. nov., tow ascomycetous yeasts from ephemeral habitats. A van Leeuwenhoek 99:241–247
Carneiro MT, Silva DM, Chagas TGP, Zahner V, Asensi MD, Hagler AN (2015) Complementary bioindicators to colorimetric assays in the water quality analysis: the potential of yeasts in Juturnaíba lake/Brazil. Sistem Gestão 10:542–552
Chang CF, Chen CC, Lee CF, Liu SM (2013) Identifying and characterizing Yarrowia keelungensis sp. nov., an oil-degrading yeast isolated from the sea surface microlayer. A van Leeuwenhoek 104:1117–1123
Chen Y-S, Yanagida F, Chen LY (2009) Isolation of marine yeasts from coastal waters of northeastern Taiwan. Aquat Biol 8:55–60
Coelho MA, Almeida JM, Martins IM, da Silva AJ, Sampaio JP (2010) The dynamics of the yeast community of the Tagus river estuary: testing the hypothesis of the multiple origins of estuarine yeasts. A van Leeuwenhoek 98:331–342
Colabella F, Moliné M, Libkind D (2014) UV Sunscreens of microbial origin: mycosporines and mycosporine-like aminoacids. Recent Pat Biotechnol 8:189–193
Cook SJ, Kougkoulos I, Edwards LA, Dortch J, Hoffmann D (2016) Glacier change and glacial lake outburst flood risk in the Bolivian Andes. Cryosphere 10:2399–2413
Cooke WEB (1976) Fungi in sewages. In: Jones EBG (ed) Recent advances in aquatic mycology. Wiley, New York, pp 389–434
Coronato F (2016) Introducing Patagonia: an approach from geo-history. In: Olivera N, Libkind D, Donati R (eds) Biology and biotechnology of patagonian microorganisms. Springer, pp 1–14
de Almeida JM (2005) Yeast community survey in the Tagus estuary. FEMS Microbiol Ecol 53:295–303
de García V, Brizzio S, Libkind D, Buzzini P, van Broock M (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol Ecol 59:331–341
de García V, Brizzio S, Libkind D, Rosa CA, van Broock M (2010a) Wickerhamomyces patagonicus sp. nov., an ascomycetous yeast species from Patagonia, Argentina. Int J Syst Evol Microbiol 60:1693–1696
de García V, Brizzio S, Russo G, Rosa CA, Boekhout T, Theelen B, Libkind D, van Broock M (2010b) Cryptococcus spencermartinsiae sp. nov., a basidiomycetous yeast isolated from glacial waters and apple fruits. Int J Syst Evol Microbiol 60:707–711
de García V, Brizzio S, van Broock MR (2012) Yeasts from glacial ice of Patagonian Andes, Argentina. FEMS Microbiol Ecol 82:540–550
de García V, Libkind D, Moliné M, Rosa CA, Giraudo MR (2014) Cold-adapted yeasts in Patagonian habitats. In: Buzzini P, Margesin R (eds) Cold adapted yeasts. Springer, Berlin, Heidelberg, pp 123–148
de García V, Coelho MA, Maia TM, Rosa LH, Vaz AM, Rosa CA, Sampaio JP, Goncalves P, van Broock M, Libkind D (2015) Sex in the cold: taxonomic reorganization of psychrotolerant yeasts in the order Leucosporidiales. FEMS Yeast Res 15:1–11
Díaz M, Pedrozo F, Baccala N (2000) Summer classification of Southern Hemisphere temperate lakes (Patagonia, Argentina). Lakes Reservoirs 5:213–229
Donachie SP, Zdanowski MK (1998) Potential digestive function of bacteria in krill Euphausia superba stomach. Aquat Microb Ecol 14:129–136
Dong X, Jiang W, Li C, Ma N, Xu Y, Meng X (2015) Patulin biodegradation by marine yeast Kodameae ohmeri. Food Addit Contam Part A 32:352–360
Ebert D, Lipsitch M, Mangin KL (2000a) The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six micro-parasites. Am Nat 156:459–477
Ebert D, Zschokke-Rohringer CD, Carius HJ (2000b) Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122:200–209
Ekendahl S, O’Neill AH, Thomsson E, Pedersen K (2003) Characterisation of yeasts isolated from deep igneous rock aquifers of the Fennoscandian Shield. Microb Ecol 46:416–428
Fell JW (1961) A new species of Saccharomyces isolated from a subtropical estuary. A van Leeuwenhoek 27:27–30
Fell JW (1967) Distribution of yeasts in the Indian Ocean. Bull Mar Sci 17:454–470
Fell JW (1970) The genus Sterigmatomyces. In: Lodder J (ed) The yeasts, a taxonomic study. North Holland, Amsterdam, pp 1229–1234
Fell JW (2012) Yeast in marine environments. In: Jones EBG, Pang K-L (eds) Marine fungi and fungal-like microorganisms marine and freshwater botany. de Gruyter, Berlin, Boston, pp 91–102
Fell JW, Hunter IL (1968) Isolation of heterothallic yeast strains of Metschnikowia Kamienski and their mating reactions with Chlamydozyma Wickerham spp. A van Leeuwenhoek 34:365–376
Fell JW, Statzell-Tallman A (1971) Sympodiomyces gen. n., a yeast-like organism from southern marine waters. A van Leeuwenhoek 37:359–367
Fell JW, Statzell-Tallman A, Scorzetti G, Gutiérrez MH (2011) Five new species of yeasts from fresh water and marine habitats in the Florida Everglades. A van Leeuwenhoek 99:533–549
Fischer B, Brebeck C (1894) Zur Morphologie, Biologie, und Systematik der Kahmpilze, der Monilia candida Hansen und des Soorerregers. C. Fischer, Jena
Fonseca A, Boekhout T, Fell JW (2011) Cryptococcus Vuillemin (1901). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 1661–1738
Frisvad JC (2008) Fungi in cold ecosystems. In: Margesin R, Schinner F, Marx JC, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, Heidelberg, pp 137–156
Furbino LE, Godinho VM, Santiago IF, Pellizzari FM, Alves TM, Zani CL, Jinion PA, Romanha AJ, Carvalho AG, Gil LH, Rosa CA, Minnis AM, Rosa LH (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic peninsula. Microb Ecol 67:775–787
Gadanho M, Sampaio JP (2002) Polyphasic taxonomy of the basidiomycetous yeast genus Rhodotorula: Rh. glutinis sensu stricto and Rh. dairenensis comb. nov. FEMS Yeast Res 2:47–58
Gadanho M, Sampaio JP (2004) Application of temperature gradient gel electrophoresis to the study of yeast diversity in the estuary of the Tagus river, Portugal. FEMS Yeast Res 5:253–261
Gadanho M, Sampaio JP (2005) Occurrence and diversity of yeasts in the Mid-Atlantic Ridge hydrothermal fields near the Azores archipelago. Microb Ecol 50:408–417
Gadanho M, Sampaio JP (2009) Cryptococcus ibericus sp. nov., Cryptococcus aciditolerans sp. nov. and Cryptococcus metallitolerans sp. nov., a new ecoclade of anamorphic basidiomycetous yeast species from an extreme environment associated with acid rock drainage in Sao Domingos pyrite mine, Portugal. Int J Syst Evol Microbiol 59:2375–2379
Gadanho M, Almeida JMF, Sampaio JP (2003) Assessment of yeast diversity in a marine environment in the south of Portugal by microsatellite-primed PCR. A van Leeuwenhoek 84:217–227
Gadanho M, Libkind D, Sampaio JP (2006) Yeast diversity in the extreme acidic environments of the Iberian Pyrite Belt. Microb Ecol 52:552–563
Gao L, Chi Z, Sheng J, Wang L, Li J, Gong F (2007) Inulinase-producing marine yeasts: evaluation of their diversity and inulin hydrolysis by their crude enzymes. Microb Ecol 54:722–729
Gao Z, Li B, Zheng C, Wang G (2008) Molecular detection of fungal communities in the Hawaiian marine sponges Suberites zeteki and Mycale armata. Appl Environ Microbiol 74:6091–6101
Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya NS, Pupo D, Alves TM, Junior PA, Romanha AJ, Zani CL, Cantrell CL, Rosa CA, Rosa LH (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451
Goh TK, Hyde KD (1996) Biodiversity of freshwater fungi. J Ind Microbiol 17:328–345
Guo FJ, Ma Y, Xu HM, Wang XH, Chi ZM (2013) A novel killer toxin produced by the marine-derived yeast Wickerhamomyces anomalus YF07b. A van Leeuwenhoek 103:737–746
Gupta A, Vongsvivut J, Barrow CJ, Puri M (2012) Molecular identification of marine yeast and its spectroscopic analysis establishes unsaturated fatty acid accumulation. J Biosci Bioeng 114:411–417
Hagler AN, Ahearn DG (1987) Ecology of aquatic yeasts. In: Rose AH, Harrison JS (eds) The yeasts, Yeasts and the environment, vol 2. Academic Press, London, pp 181–205
Hagler AN, Mendonça-Hagler LC (1981) Yeasts from marine and estuarine waters with different levels of pollution in the state of Rio de Janeiro, Brazil. Appl Environ Microbiol 41:173–178
Hagler AN, Mendonça-Hagler LC, Santos EA, Farage S, Silva Filho JB, Schrank A, de Oliveira RB (1986) Microbial pollution indicators in Brazilian tropical and subtropical marine surface waters. Sci Total Environ 15:151–160
Hassanshahian M, Tebyanian H, Cappello S (2012) Isolation and characterization of two crude oil-degrading yeast strains, Yarrowia lipolytica PG-20 and PG-32, from the Persian Gulf. Mar Pollut Bull 64:1386–1391
Inácio J, Pereira P, de Carvalho M, Fonseca Á, Amaral-Collaço MT, Spencer-Martins I (2002) Estimation and diversity of phylloplane mycobiota on selected plants in a Mediterranean-type ecosystem in Portugal. Microb Ecol 44:344–353
Ishida S, Nozaki D, Grossart HP, Kagami M (2015) Novel basal, fungal lineages from freshwater phytoplankton and lake samples. Environ Microbiol Rep 7:435–441
Jebaraj CS, Raghukumar C, Behnke A, Stoeck T (2010) Fungal diversity in oxygen-depleted regions of the Arabian Sea revealed by targeted environmental sequencing combined with cultivation. FEMS Microbiol Ecol 71:399–412
Jin L, Liu F, Sun W, Zhang F, Karuppiah V, Li Z (2014) Pezizomycotina dominates the fungal communities of South China Sea sponges Theonella swinhoei and Xestospongia testudinaria. FEMS Microbiol Ecol 90:935–945
Jones EBG, Slooff WC (1966) Candida aquatica sp. nov. isolated from water scums. A van Leeuvenhoek 32:223–228
Jones G, Southworth EB, Libkind D, Marvanová L (2014) Freshwater basidiomycota. In: Jones G, Pang K-L, Hyde K (eds) Freshwater fungi and fungus-like organisms. De Gruyter, Berlin, pp 73–108
Kandasamy K, Alikunhi NM, Subramanian M (2012) Yeasts in marine and estuarine environments. J Yeast Fungal Res 3:74–82
Kurtzman CP, Fell JW (2004) Yeast. In: Muller GM, Bills GF, Foster MS (eds) Biodiversity of fungi. Elsevier Academic Press, London, pp 337–342
Kurtzman CP, Fell JW (2006) Yeast systematics and phylogeny-implications of molecular identification methods for studies in ecology. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 11–30
Kutty SN, Philip R (2008) Marine yeasts – a review. Yeast 25:465–483
Kwasniewska K (1988) Horizontal distribution and density of yeasts and filamentous fungi in lake St. Clair water. J Great Lakes Res 14:438–443
Lachance MA (2011a) Kluyveromyces van der Walt (1971). In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, pp 471–482
Lachance MA (2011b) Metschnikowia Kamienski (1899). In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, pp 575–621
Lachance MA, Starmer WT (1998) Ecology and yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, pp 21–30
Last FT, Price D (1969) Yeasts associated with living plants and their environs. In: Rose AH, Harrison JS (eds) The yeasts. Academic Press, New York, pp 183–218
Le Calvez T, Burgaud G, Mahé S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep-sea hydrothermal ecosystems. Appl Environ Microbiol 75:6415–6421
Lefèvre E, Bardot C, Noël C, Carrias JF, Viscogliosi E, Amblard C, Sime-Ngando T (2007) Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ Microbiol 9:61–71
Lewis WM (2000) Basis for the protection and management of tropical lakes. Lakes Reserv Res Manag 5(1):35–48
Li X, Chi Z, Liu Z, Yan K, Li H (2008) Phytase production by a marine yeast Kodamaea ohmeri BG3. Appl Biochem Biotechnol 149:183–193
Li J, Peng Y, Wang X, Chi Z (2010a) Optimum production and characterization of an acid protease from marine yeast Metschnikowia reukaufii W6b. J Ocean Univ China 9:359–364
Li M, Liu G-L, Chi Z, Chi Z-M (2010b) Single cell oil production from hydrolysate of cassava starch by marine-derived yeast Rhodotorula mucilaginosa TJY15a. Biomass Bioenergy 34:101–107
Libkind D, Brizzio S, Ruffini A, Gadanho M, van Broock MR, Sampaio JP (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. A van Leeuwenhoek 84:313–322
Libkind D, Brizzio S, van Broock M (2004a) Rhodotorula mucilaginosa, a carotenoid producing yeast strain from a Patagonian high-altitude lake. Folia Microbiol 49:19–25
Libkind D, Perez P, Sommaruga R, Dieguez MC, Ferraro M, Brizzio S, Zagarese H, van Broock M (2004b) Constitutive and UV-inducible synthesis of photoprotective compounds (carotenoids and mycosporines) by freshwater yeasts. Photochem Photobiol Sci 3:281–286
Libkind D, Sommaruga R, Zagarese H, van Broock M (2005a) Mycosporines in carotenogenic yeasts. Syst Appl Microbiol 28:749–754
Libkind D, Gadanho M, van Broock M, Sampaio JP (2005b) Sporidiobolus longiusculus sp. nov. and Sporobolomyces patagonicus sp. nov., novel yeasts of the Sporidiobolales isolated from aquatic environments in Patagonia, Argentina. Int J Syst Evol Microbiol 55:503–509
Libkind D, Dieguez MC, Moliné M, Perez P, Zagarese HE, van Broock M (2006) Occurrence of photoprotective compounds in yeasts from freshwater ecosystems of northwestern Patagonia (Argentina). Photochem Photobiol 82:972–980
Libkind D, Ruffini A, van Broock M, Alves L, Sampaio JP (2007) Biogeography, host-specificity, and molecular phylogeny of Phaffia rhodozyma and its sexual form, Xanthophyllomyces dendrorhous. Appl Environ Microbiol 73:1120–1125
Libkind D, Gadanho M, van Broock M, Sampaio JP (2008) Studies on the heterogeneity of the carotenogenic yeast from Patagonia, Argentina. J Basic Microbiol 48(2):93–98
Libkind D, Moliné M, Sampaio JP, van Broock M (2009a) Yeasts from high-altitude lakes: influence of UV radiation. FEMS Microbiol Ecol 69:353–362
Libkind D, Gadanho M, van Broock M, Sampaio JP (2009b) Cystofilobasidium lacus-mascardii sp. nov., a basidiomycetous yeast species isolated from aquatic environments of the Patagonian Andes, and Cystofilobasidium macerans sp. nov., the sexual stage of Cryptococcus macerans. Int J Syst Evol Microbiol 59:622–630
Libkind D, Sampaio JP, van Broock M (2010) Cystobasidiomycetes yeasts from Patagonia (Argentina): description of Rhodotorula meli sp. nov. from glacial meltwater. Int J Syst Evol Microbiol 60:2251–2256
Libkind D, Hittinger CT, Valerio E, Goncalves C, Dover J, Johnston M, Goncalves P, Sampaio JP (2011a) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci U S A 108:14539–14544
Libkind D, Moliné M, Sommaruga R, Sampaio JS, van Broock M (2011b) Phylogenetic distribution of fungal mycosporines within Pucciniomycotina (Basidiomycota). Yeast 28:619–627
Libkind D, Moliné M, van Broock M (2011c) Production of the UVB absorbing compound Mycosporine-glutaminol-glucoside by Xanthophyllomyces dendrorhous (Phaffia rhodozyma). FEMS Yeast Res 11:52–59
Libkind D, Tognetti C, Ruffini A, Sampaio JP, van Broock M (2011d) Xanthophyllomyces dendrorhous (Phaffia rhodozyma) on stromata of Cyttaria hariotii in Patagonian Nothofagus forests. Rev Argent Microbiol 43:226–232
Libkind D, Moliné M, Bellora N, Trochine A, de García V (2016) Patagonian yeasts of biotechnological relevance. In: Olivera N, Libkind D, Donati R (eds) Biology and biotechnology of patagonian microorganisms. Springer, pp 325–351
Lorenz R, Molitoris HP (1997) Cultivation of fungi under simulated deep sea conditions. Mycol Res 101:1355–1365
Loureiro STA, de Queiroz-Cavalcanti MA, Neves RP, de Oliveira Passavante JZ (2005) Yeasts isolated from sand and sea water in beaches of Olinda, Pernambuco state, Brazil. Braz J Microbiol 36:1–8
Madhour A, Anke H, Mucci A, Davoli P, Weber RW (2005) Biosynthesis of the xanthophyll plectaniaxanthin as a stress response in the red yeast Dioszegia (Tremellales, Heterobasidiomycetes, Fungi). Phytochemistry 66:2617–2626
Medeiros AO, Kohler LM, Hamdan JS, Missagia BS, Barbosa FA, Rosa CA (2008) Diversity and antifungal susceptibility of yeasts from tropical freshwater environments in Southeastern Brazil. Water Res 42:3921–3929
Medeiros AO, Missagia BS, Brandão LR, Callisto M, Barbosa FA, Rosa CA (2012) Water quality and diversity of yeasts from tropical lakes and rivers from the Rio Doce basin in Southeastern Brazil. Braz J Microbiol 43:1582–1594
Mestre MC, Rosa CA, Safar SV, Libkind D, Fontenla SB (2011) Yeast communities associated with the bulk-soil, rhizosphere and ectomycorrhizosphere of a Nothofagus pumilio forest in northwestern Patagonia, Argentina. FEMS Microbiol Ecol 78:531–541
Meyers SP, Ahearn DG, Cooke WL (1970) Mycological studies of lake Champlain. Mycologia 62:504–515
Meyers SP, Ahearn DG, Alexander SK, Cook WL (1975) Pichia spartinae, dominant yeast of the Spartina salt marsh. Dev Ind Microbiol 16:262–267
Miller MW, Phaff HJ (1998) Metschnikowia kamienski. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, pp 256–267
Modenutti BE, Balseiro EG, Queimaliños CP, Añon Suarez D, Diéguez MC, Albariño RJ (1998) Structure and dynamics of food web Andean lakes. Lakes Reserv Res Manag 3:179–186
Moliné M (2004) Carotenogénesis: efecto de la radiación ultravioleta sobre levaduras pigmentadas. Undergraduate Thesis. Universidad Nacional del Comahue, Bariloche, Argentina
Moliné M (2010) Producción de compuestos fotoprotectores (carotenoides y micosporinas) por levaduras. PhD thesis, Universidad Nacional de Tucumán, Tucumán, Argentina
Moliné M, Libkind D, Dieguez M d C, van Broock M (2009) Photoprotective role of carotenoids in yeasts: response to UV-B of pigmented and naturally-occurring albino strains. J Photochem Photobiol B 95:156–161
Moliné M, Flores MR, Libkind D, Dieguez M d C, Farias ME, van Broock M (2010) Photoprotection by carotenoid pigments in the yeast Rhodotorula mucilaginosa: the role of torularhodin. Photochem Photobiol Sci 9:1145–1151
Moliné M, Arbeloa EM, Flores MR, Libkind D, Farías ME, Bertolotti SG, Churio MS, van Broock MR (2011) UVB photoprotective role of mycosporines in yeast: photostability and antioxidant activity of mycosporine-glutaminol-glucoside. Radiat Res 175:44–50
Monchy S, Sanciu G, Jobard M, Rasconi S, Gerphagnon M, Chabé M, Cian A, Meloni D, Niquil N, Christaki U, Viscogliosi E, Sime-Ngando T (2011) Exploring and quantifying fungal diversity in freshwater lake ecosystems using rDNA cloning/sequencing and SSU tag pyrosequencing. Environ Microbiol 13:1433–1453
Moore MM, Strom MS (2003) Infection and mortality by the yeast Metschnikowia bicuspidate var. bicuspidate in Chinook salmon fed live adult brine shrimp (Artemia franciscana). Aquaculture 220:43–57
Morais P, Resende MA, Rosa CA, Barbosa FAR (1996) Occurrence and diel distribution of yeast in a paleo-karstic lake of Southeastern Brazil. Rev Microbiol 27:182–188
Mouton M, Postma F, Wilsenach J, Botha A (2012) Diversity and characterization of culturable fungi from marine sediment collected from St. Helena Bay, South Africa. Microb Ecol 64:311–319
Nagahama T (2006) Yeast biodiversity in freshwater, marine and deep-sea environments. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 241–262
Nagahama T, Hamamoto M, Nakase T, Horikoshi K (1999) Kluyveromyces nonfermentans sp. nov., a new yeast species isolated from the deep sea. Int J Syst Bacteriol 49:1899–1905
Nagahama T, Hamamoto M, Nakase T, Takami H, Horikoshi K (2001a) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. A van Leeuwenhoek 80:101–110
Nagahama T, Hamamoto M, Nakase T, Horikoshi K (2001b) Rhodotorula lamellibrachii sp. nov., a new yeast species from a tubeworm collected at the deep-sea floor in Sagami bay and its phylogenetic analysis. A van Leeuwenhoek 80:317–323
Nagahama T, Hamamoto M, Nakase T, Horikoshi K (2003a) Rhodotorula benthica sp. nov. and Rhodotorula calyptogenae sp. nov., novel yeast species from animals collected from the deep-sea floor, and Rhodotorula lysiniphila sp. nov., which is related phylogenetically. Int J Syst Evol Microbiol 53:897–903
Nagahama T, Hamamoto M, Nakase T, Takaki Y, Horikoshi K (2003b) Cryptococcus surugaensis sp. nov., a novel yeast species from sediment collected on the deep-sea floor of Suruga Bay. Int J Syst Evol Microbiol 53:2095–2098
Nagahama T, Hamamoto M, Horikoshi K (2006) Rhodotorula pacifica sp. nov., a novel yeast species from sediment collected on the deep-sea floor of the north-west Pacific Ocean. Int J Syst Evol Microbiol 56:295–299
Nagano Y, Nagahama T, Hatada Y, Nonoura T, Takami H, Miyazaki J, Takai K, Horikoshi K (2010) Fungal diversity in deep-sea sediments – the presence of novel fungal groups. Fungal Ecol 3:316–325
Nagy E, Niss M, Dlauchy D, Arneborg N, Nielsen DS, Péter G (2013) Yarrowia divulgata f.a., sp. nov., a yeast species from animal-related and marine sources. Int J Syst Evol Microbiol 63:4818–4823
Nagy E, Dlauchy D, Medeiros AO, Péter G, Rosa CA (2014) Yarrowia porcina sp. nov. and Yarrowia bubula f.a., sp. nov., two yeast species form meat and river sediment. A van Leeuwenhoek 105:697–707
Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10
Pagnocca FC, Mendonca-Hagler LC, Hagler AN (1989) Yeasts associated with the white shrimp Penaeus schmitti, sediment and water of Sepetiba Bay, Rio de Janeiro, Brazil. Yeast 5:5479–5483
Papadakis JS, Mavridou A, Richardson SC, Lamprini M, Marcelou U (1997) Bather-related microbial and yeast populations in sand and seawater. Water Res 31:799–804
Pedrozo F, Chillrud S, Temporetti P, Diaz M (1993) Chemical composition and nutrient limitation in rivers and lakes of northern Patagonian Andes (39.5° – 42° S; 71° W) (Rep. Argentina). Verh Internat Verein Limnol 25:207–214
Pore RS, Sorenson WG (1990) Reniforma strues, a new yeast from wastewater. Mycologia 82:549–553
Prabhakaran N, Gupta R (1991) Yeasts from the sediment samples of the EEZ along the southwest coast of India. J Mar Biol Assoc India 33:455
Quirós R, Drago E (1985) Relaciones entre variables físicas, morfométricas y climáticas en lagos patagónicos. Rev Asoc Cienc Nat Litoral 16:181–199
Reche I, Pulido-Villena E, Morales-Baquero R, Casamayor EO (2005) Does ecosystem size determine aquatic bacterial richness? Ecology 86:1715–1722
Rédou V, Navarri M, Meslet-Cladière L, Barbier G, Burgaud G (2015) Species richness and adaptation of marine fungi from deep-subseafloor sediments. Appl Environ Microbiol 81:3571–3583
Rosa CA, Resende MA, Franzot SP, Morais PB, Barbosa FAR (1990) Yeasts and coliform distribution in a paleokarstic lake of Lagoa-Santa Plateau-MG, Brazil. Rev Microbiol 21:19–24
Rosa CA, Resende MA, Barbosa FAR, Morais PB, Franzot SP (1995) Yeast diversity in a mesotrophic lake on the karstic plateau of Lagoa Santa, MG-Brazil. Hydrobiology 308:103–108
Roth FJ, Ahearn DG, Fell JW, Meyew SP, Meyer SA (1962) Ecology and taxonomy of yeasts isolated from various marine substrates. Limnol Oceanogr 2:178–185
Russo G, Libkind D, Sampaio JP, van Broock MR (2008) Yeast diversity at the Volcanic acidic environment of the Lake Caviahue and Rio Agrio (Patagonia, Argentina). FEMS Microbiol Ecol 65:415–424
Russo G, Libkind D, Ulloa RJ, de García V, Sampaio JP, van Broock MR (2010) Cryptococcus agrionensis sp. nov., a basidiomycetous yeast of the acidic rock drainage ecoclade, isolated from acidic aquatic environments of volcanic origin (River Agrio, Argentina). Int J Syst Evol Microbiol 60:996–1000
Russo G, Libkind D, Giraudo MR, Delgado O (2016) Metal capture by autochthonous yeasts from a volcanic influenced environment of Patagonia. J Basic Microbiol 56:1203–1211
Sabino R, Verissimo C, Cunha MA, Wergikoski B, Ferreira FC, Rodrigues R, Prada H, Falcao L, Rosado L, Pinheiro C, Paixao E, Brandão J (2011) Pathogenic fungi: an unacknowledged risk at coastal resorts? New insights on microbiological sand quality in Portugal. Mar Pollut Bull 62:1506–1511
Sampaio JP (2004) Diversity, phylogeny and classification of basidiomycetous yeasts. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers in Basidiomycota mycology. IHW Verlag, Eching, Germany, pp 49–80
Sampaio JP (2011) Rhodosporidium Banno (1967). In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, pp 1523–1539
Sampaio A, Sampaio JP, Leão C (2007) Dynamics of yeast populations recovered from decaying leaves in a nonpolluted stream: a 2-year study on the effects of leaf litter type and decomposition time. FEMS Yeast Res 7:595–603
Seki H, Fulton J (1969) Infection of marine copepods by Metschnikowia sp. Mycopathol Mycol Appl 38:61–70
Seshadri R, Sieburth J (1971) Cultural estimation of yeasts on seaweeds. Appl Microbiol 22:507–512
Shearer CA, Descals E, Kohlmeyer B, Kohlmeyer J, Marvanová L, Padgett D, Porter D, Raja HA, Schmit JP, Thorton HA, Voglymayr H (2007) Fungal biodiversity in aquatic habitats. Biodivers Conserv 16:49–67
Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262
Siepmann R, Hohnk W (1962) Uber Hefen und einige Pilze (Fungi imp., Hyphales) aus dem Nordatlantik. Veroeff Inst Meeresforsch Bremerhaven 8:79–97
Silva-Bedoya LM, Ramírez-Castrillón M, Osório-Cadavid E (2014) Yeast diversity associated to sediments and water from two Colombian artificial lakes. Braz J Microbiol 45:135–142
Simard RE, Blackwood AC (1971a) Ecological studies on yeasts in the St Lawrence River. Can J Microbiol 17:353–357
Simard RE, Blackwood AC (1971b) Yeasts from the St. Lawrence River. Can J Microbiol 17:197–203
Singh P, Raghukumar C, Meena RM, Verma P, Shouche Y (2012a) Fungal diversity in deep-sea sediments revealed by culture-dependent and culture-independent approaches. Fungal Ecol 5:543–553
Singh P, Raghukumar C, Verma P, Shouche Y (2012b) Assessment of fungal diversity in deep-sea sediments by multiple primer approach. World J Microbiol Biotechnol 28:659–667
Sláviková E, Vadkertiová R (1997) Seasonal occurrence of yeasts and yeast-like organisms in the river Danube. A van Leeuwenhoek 72:77–80
Slávikova E, Vadkertiova R (2000) The occurrence of yeasts in the forest soils. J Basic Microbiol 40:207–212
Sláviková E, Vadkertiová R, Kocková-Kratochvílová A (1992) Yeasts isolated from artificial lake waters. Can J Microbiol 38:1206–1209
Soares CAG, Maury M, Pagnocca FC, Araujo FV, Mendonca-Hagler LC, Hagler AN (1997) Ascomycetous yeasts from tropical intertidal dark mud of southeast Brazilian estuaries. J Gen Appl Microbiol 43:265–272
Sommaruga R, Libkind D, van Broock M, Whitehead K (2004) Mycosporine-glutaminolglucoside, a UV-absorbing compound of two Rhodotorula yeast species. Yeast 21:1077–1081
Spencer JFT, Spencer DM (1997) Yeasts in natural and artificial habitat. Springer, Berlin
Statzell-Tallman A, Belloch C, Fell JW (2008) Kwoniella mangroviensis gen. nov., sp. nov. a tremellaceous yeast from mangrove habitats in the Florida Everglades and Bahamas. FEMS Yeast Res 8:103–113
Stone W, Jones BL, Wilsenach J, Botha A (2012) External ecological niche for Candida albicans within reducing, oxygen-limited zones of wetlands. Appl Environ Microbiol 78:2443–2445
Takishita K, Tsuchiya M, Reimer JD, Maruyama T (2006) Molecular evidence demonstrating the basidiomycetous fungus Cryptococcus curvatus is the dominant microbial eukaryote in sediment at the Kuroshima Knoll methane seep. Extremophiles 10:165–169
Takishita K, Yubuki N, Kakizoe N, Inagaki Y, Maruyama T (2007) Diversity of microbial eukaryotes in sediment at a deep-sea methane cold seep: surveys of ribosomal DNA libraries from raw sediment samples and two enrichment cultures. Extremophiles 11:563–576
Torres A, Hochberg M, Pergament I, Smoum R, Niddam V, Dembitsky VM, Temina M, Dor I, Lev O, Srebnik M, Enk CD (2004) A new UV-B absorbing mycosporine with photo protective activity from the lichenized ascomycete Collema cristatum. Eur J Biochem 271:780–784
Valente P, Boekhout T, Landell MF, Crestani J, Pagnocca FC, Sette LD, Passarini MR, Rosa CA, Brandão LR, Pimenta RS, Ribeiro JR, García KM, Lee CF, Suh SO, Péter G, Dlauchy D, Fell JW, Scorzetti G, Theelen B, Vainstein MH (2012) Bandoniozyma gen. nov., a genus of fermentative and non-fermentative tremellaceous yeast species. PLoS One 7:e46060
van Uden N, Ahearn DC (1963) Occurrence and population densities of yeast species in a fresh-water lake. A van Leeuwenhoek 29:308–312
van Uden N, Castelo-Branco R (1961) Metschnikowiella zobellii sp. nov. and M. krissii sp. nov. two yeasts from the Pacific Ocean pathogenic for Daphnia magna. J Gen Microbiol 26:141–148
van Uden N, ZoBell CE (1962) Candida marina nov. spec., Torulopsis torresii nov. spec. and T. maris nov. spec., three yeasts from the Torres Strait. A van Leeuwenhoek 28:275–283
Vaz ABM, Rosa LH, Vieira MLA, de Garcia V, Brandão LR, Teixeira LCRS, Moliné M, Libkind D, van Broock M, Rosa CA (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 42:937–947
Velegraki-Abel V, Marselou-Kinti U, Richardson D (1987) Incidence of yeasts in coastal sea water of the Attica Peninsula, Greece. Water Res 21:1363–1369
Villafañe VE, Helbling WE, Zagarese HE (2001) Solar ultraviolet radiation and its impact on aquatic systems of Patagonia, South America. Ambio 30:112–117
Vogel C, Rogerson A, Schatz S, Laubach H, Tallman A, Fell J (2007) Prevalence of yeasts in beach sand at three bathing beaches in South Florida. Water Res 41:1915–1920
Wang L, Chi Z, Wang X, Ju L, Chi Z, Guo N (2008) Isolation and characterization of Candida membranifaciens subsp. flavinogenie W14-3, a novel riboflavin-producing marine yeast. Microbiol Res 163:255–266
Wurzbacher C, Bärlocher F, Grossart H-P (2010) Fungi in lake ecosystems. Aquat Microb Ecol 59:125–149
Xu W, Pang KL, Luo ZH (2014) High fungal diversity and abundance recovered in the deep-sea sediments of the Pacific Ocean. Microb Ecol 68:688–698
Xu W, Luo Z-H, Guo S, Pang K-L (2016) Fungal community analysis in the deep-sea sediments of the Pacific Ocean assessed by comparison of ITS,18S and 28S ribosomal DNA regions. Deep-Sea Res 109:51–60
Yamaguchi K, Degawa Y, Nakagiri A (2009) An aero-aquatic fungus, Peyronelina glomerulata, is shown to have teleomorphic affinities with cyphelloid basidiomycetes. Mycoscience 50:156–164
Yamasato K, Goto S, Ohwada K, Okuno D, Araki H, Iizuka H (1974) Yeasts from the Pacific Ocean. J Gen Appl Microbiol 20:289–307
Yang S-P, Wu Z-H, Jian J-C (2011) Distribution of marine red yeasts in shrimps and the environments of shrimp culture. Curr Microbiol 62:1638–1642
Yurkov AM (2017) Temporal and geographic patterns in yeast distribution. In: Buzzini P, Lachance MA, Yurkov AM (eds) Yeasts in natural ecosystems: ecology. Springer, Heidelberg, pp 101–130
Yurkov AM, Pozo MI (2017) Yeast community composition and structure. In: Buzzini P, Lachance MA, Yurkov AM (eds) Yeasts in natural ecosystems: ecology. Springer, Heidelberg, pp 73–100
Yurkov AM, Kachalkin AV, Daniel HM, Groenewald M, Libkind D, de García V, Zalar P, Gouliamova DE, Boekhout T, Begerow D (2015) Two yeast species Cystobasidium psychroaquaticum f.a. sp. nov. and Cystobasidium rietchieii f.a. sp. nov. isolated from natural environments, and the transfer of Rhodotorula minuta clade members to the genus Cystobasidium. A van Leeuwenhoek 107:173–185
Zhang XY, Tang GL, Xu XY, Nong XH, Qi SH (2014) Insights into deep-sea sediment fungal communities from the East Indian Ocean using targeted environmental sequencing combined with traditional cultivation. PLoS One 9:e109118
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Libkind, D., Buzzini, P., Turchetti, B., Rosa, C.A. (2017). Yeasts in Continental and Seawater. In: Buzzini, P., Lachance, MA., Yurkov, A. (eds) Yeasts in Natural Ecosystems: Diversity. Springer, Cham. https://doi.org/10.1007/978-3-319-62683-3_1
Download citation
DOI: https://doi.org/10.1007/978-3-319-62683-3_1
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-62682-6
Online ISBN: 978-3-319-62683-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)