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Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential

Pietro Buzzini , Eva Branda , Marta Goretti , Benedetta Turchetti
DOI: http://dx.doi.org/10.1111/j.1574-6941.2012.01348.x 217-241 First published online: 1 November 2012

Abstract

Glacial habitats (cryosphere) include some of the largest unexplored and extreme biospheres on Earth. These habitats harbor a wide diversity of psychrophilic prokaryotic and eukaryotic microorganisms. These highly specialized microorganisms have developed adaptation strategies to overcome the direct and indirect life-endangering influence of low temperatures. For many years Antarctica has been the geographic area preferred by microbiologists for studying the diversity of psychrophilic microorganisms (including yeasts). However, there have been an increasing number of studies on psychrophilic yeasts sharing the non-Antarctic cryosphere. The present paper provides an overview of the distribution and adaptation strategies of psychrophilic yeasts worldwide. Attention is also focused on their biotechnological potential, especially on their exploitation as a source of cold-active enzymes and for bioremediation purposes.

Keywords
  • glacial environments
  • psychrophilic yeasts
  • yeast diversity
  • adaptation strategies
  • biotechnological potential

Introduction

Over 80% of the Earth's biosphere is permanently or periodically exposed to temperatures below 5 °C (Cavicchioli & Tortsen 2000, Margesin et al., 2007a, b). Cold environments include deep seas (90% of the oceans exhibit temperatures < 5 °C), cold deserts and glacial habitats (Margesin & Miteva, 2011). Glacial habitats (cryosphere) are characterized by the presence of ice in extensive masses. They cover about 10% of the Earth's surface at the present time and include glaciers (and related habitats), icy seas, ice caps and continental ice sheets, and frozen ground (Paterson, 1994; Benn & Evans, 1998). A few excellent inventories of the global cryosphere have been recently published [IGOS (Integrated Global Observing Strategy), 2007; WGMS (World glacier monitoring service), 2007]. Glacial habitats harbor a wide diversity of psychrophilic prokaryotic and eukaryotic microbial life, including archaea, bacteria, cyanobacteria, yeasts, filamentous fungi, algae and protozoa. These highly specialized microorganisms have developed some adaptation strategies to overcome the direct and indirect life-endangering influence of low temperatures (Staley & Gosink, 1999; Christner et al., 2000; Ma et al., 2000; Poglazova et al., 2001; Deming, 2002; Gunde-Cimerman et al., 2003; Mader et al., 2006; Margesin et al., 2007a, b; Margesin & Miteva, 2011).

Conventionally, cold-adapted microorganisms can be divided into obligate and facultative psychrophiles. Obligate psychrophiles exhibit an optimal temperature for growth around 15 °C, a maximum temperature ≤ 20 °C and a minimal temperature for growth at 0 °C or lower (Morita, 1975; Arthur & Watson, 1976). In contrast, microorganisms growing at 0 °C but exhibiting optimal temperature for growth at 20–30 °C are designated facultative psychrophiles (psychrotolerant) (Vishniac, 1987; Cavicchioli & Tortsen, 2000; Raspor & Zupan, 2006). Facultative psychrophiles have evolved to tolerate cold, but they are not as physiologically specialized as obligate psychrophiles: the former are generally predominant in ecosystems periodically exposed to low temperatures whereas the latter predominate in permanent glacial habitats (e.g. polar regions) (Gounot, 1986; Cavicchioli & Tortsen, 2000). However, in some cases (e.g. in Antarctic soils and rocks, which are subjected to wide thermal fluctuations) facultative psychrophiles dominate (Zucconi et al., 1996). Both are believed to play key roles in the biodegradation of organic matter and the cycling of essential nutrients at the cryosphere level (Russell, 1990; Vishniac, 2006a; Shivaji & Prasad, 2009).

As recently underlined by Shivaji & Prasad (2009), yeasts are a versatile group of eukaryotic microorganisms exhibiting heterogeneous nutritional profiles and a surprising ability of survive in a wide range of natural and altered habitats (Hagler & Ahearn, 1987; Walker, 1998; Starmer & Lachance, 2011). It has even been suggested that yeasts could be better adapted to low temperatures than bacteria (Margesin et al., 2003; Turkiewicz et al., 2003).

For many years Antarctica has been the geographic area preferred by microbiologists for studying the diversity of psychrophilic microorganisms (including yeasts). As a result, only the diversity of Antarctic psychrophilic yeasts has been exhaustively reviewed (Vishniac, 2006a; Onofri et al., 2007; Shivaji & Prasad, 2009). However, an increasing number of studies on psychrophilic yeast populations sharing the non-Antarctic cryosphere have been recently reported. Hence, the literature published to date gives only a fragmentary picture about the diversity of psychrophilic yeasts in worldwide glacial habitats, as well as on their physiological and biotechnological features.

The present paper provides an overview of the diversity and adaptation strategies of psychrophilic yeast populations sharing the worldwide cryosphere. Attention is also given to the biotechnological potential of these organisms, with special emphasis on their exploitation as a source of cold-active enzymes and for bioremediation purposes.

Diversity and ecology of psychrophilic yeasts in worldwide glacial habitats

As ecological studies of psychrophilic yeasts sharing the global cryosphere have been carried out over no more than 60 years, original strain identification was performed using taxonomic criteria of current use at the time of isolation: hence, many designations could be either not adjourned or incorrect. Accordingly, all original taxonomic designations reported in the literature were checked (and, if necessary, updated) according to the latest taxonomic guidelines reported by Kurtzman et al. (2011).

Psychrophilic yeasts in Antarctica

Antarctica has an area of 14 million square kilometers: about 99% is covered by ice and snow (Holdgate, 1977; Shivaji & Prasad, 2009). The study of Antarctic yeasts has attracted considerable interest since the 1960s, because of its extremely harsh climatic conditions (di Menna, 1960, 1966a, b; Soneda, 1961; Sinclair & Stokes, 1963; Jacobs & Shafer, 1964; Goto et al., 1969; Baker, 1970a, b; Cameron, 1971; Atlas et al., 1978). Such investigations were made possible by the availability of a number of Antarctic scientific stations. Therefore, hundreds of isolates have been characterized and several novel species have been described for the first time. The list of yeast species isolated from Antarctica is summarized in Table 1. The taxonomic positions of a considerable number of species are now obsolete (Kurtzman et al., 2011). Overall, Antarctic yeasts were identified as belonging to 70 species (13 ascomycetes and 57 basidiomycetes). Yeast-like organisms (Aureobasidium pullulans) were also found: the main genus represented was Cryptococcus (about 25% of the total number of species). Overall, just a few species showed any random distribution. Soil collected from different Antarctic sites was the most common source of isolates (Table 1).

View this table:

List of yeast species isolated from Antarctica: original taxonomic designations reported in the literature were updated according to the latest taxonomic guidelines (Kurtzman et al., 2011)

SpeciesOriginal taxonomic designationIsolation sourceLocalityReference(s)
Ascomycetous yeasts
Candida intermediaAntarctic soilAlexander Island, Antarctic PeninsulaBridge & Newsham (2009)
Candida parapsilosisDecaying wood; up-wind snow and ice coresAmundsen-Scott Station, South Pole; Ross Island, Ross Sea BayJacobs & Shafer (1964), Arenz et al. (2006)
Candida psychrophilaTorulopsis psychrophilaPenguin-dung sampleDry Valleys, South Victoria LandGoto et al. (1969)
Candida rugosaAntarctic soilVictoria Landdi Menna (1966b)
Candida saitoanaTorulopsis candidaAntarctic soilVictoria Landdi Menna (1966b)
Candida sakèCandida australis; Torulopsis austromarinaPenguin-dung sample; seawaterAntarctic coast of Indo-Pacific and Indian Ocean; Dry Valleys, South Victoria LandGoto et al. (1969), Fell & Hunter (1974)
Clavispora lusitaniaeCandida lusitaniaeAntarctic soilDry Valleys, South Victoria LandBaublis et al. (1991), Connell et al. (2008)
Debaryomyces hanseniiCandida famata; Debaryomyces kloeckerii; Torulopsis famataAntarctic soil; decaying wood; moulting feathers of penguinsDry Valleys, South Victoria Land; Livingston Island, Antarctic Peninsula; Ross Island, Ross Sea Bay; Schirmacher Oasis, Queen Maud Land; Showa Base, East Ongul Island, Lutzow-Holm BaySoneda (1961), di Menna (1966b), Ray et al. (1992), Arenz et al. (2006), Connell et al. (2008), Pavlova et al. (2009)
Debaryomyces subglobosusAntarctic soilVictoria Landdi Menna (1966b)
Dipodascus australiensisDecaying woodRoss Island, Ross Sea BayArenz et al. (2006)
Galactomyces candidusGeotrichum candidumAntarctic soilDry Valleys, South Victoria LandBaublis et al. (1991)
Pichia kudriavzeviiCandida kruseiAntarctic soilDry Valleys, South Victoria LandBaublis et al. (1991)
Trichomonascus ciferriiCandida ciferriiAntarctic soilDry Valleys, South Victoria LandBaublis et al. (1991)
Basidiomycetous yeasts
Bulleromyces albusBullera albaAntarctic soil; decaying woodRoss Island, Ross Sea Bay; Schirmacher Oasis, Queen Maud LandRay et al. (1992), Arenz et al. (2006)
Cryptococcus adeliensisCryptococcus adeliaeDecayed algae in the icepackAntarctic Station Dumont d'Urville, Adélie LandPetrescu et al. (2000), Scorzetti et al. (2000)
Cryptococcus albidosimilisAntarctic soil; decaying woodDry Valleys, South Victoria Land; Linnaeus Terrace and University Valley, South Victoria Land; Ross Island, Ross Sea BayVishniac & Kurtzman (1992), Arenz et al. (2006), Connell et al. (2008)
Cryptococcus albidusAntarctic soil; ice cores; lake water; lichen and moss samplesBrown Peninsula, Ross Ice Shelf; Dry Valleys, South Victoria Land; Livingston Island, Antarctic Peninsula; McMurdo Station, Ross Island, Ross Sea Bay; Vostok Research Station; West Ongul Island, Lutzow-Holm BaySoneda (1961), di Menna (1966b), Goto et al. (1969), Cameron (1971), Atlas et al. (1978), Baublis et al. (1991), Abyzov (1993), Pavlova et al. (2009)
Cryptococcus antarcticusAntarctic soil; decaying woodLinnaeus Terrace and University Valley, South Victoria Land; Ross Island, Ross Sea BayVishniac & Kurtzman (1992), Vishniac & Onofri (2002), Arenz et al. (2006)
Cryptococcus carnescensAntarctic soil; decaying woodDry Valleys, South Victoria Land; Ross Island, Ross Sea BayArenz et al. (2006), Connell et al. (2008)
Cryptococcus diffluensAntarctic soilVictoria Landdi Menna (1966b)
Cryptococcus flavusMoulting feathers of penguinsLivingston Island, Antarctic PeninsulaPavlova et al. (2009)
Cryptococcus friedmanniiDecaying wood; rock cryptoendolithic habitatRoss Desert, South Victoria Land; Ross Island, Ross Sea BayVishniac (1985a), Arenz et al. (2006)
Cryptococcus humicolaCandida humicolaAntarctic soil; lake waterDry Valleys, South Victoria Land; Schirmacher Oasis, Queen Maud LandGoto et al. (1969), Ray et al. (1992)
Cryptococcus laurentiiAntarctic soil; decaying wood; moulting feathers of penguinsDry Valleys, South Victoria Land; Livingston Island, Antarctic Peninsula; Ross Island, Ross Sea ay; Showa Base, Est Ongul Island, Lutzow-Holm BaySoneda (1961), di Menna (1966b), Vishniac & Hempfling (1979a), Arenz et al. (2006), Pavlova et al. (2009)
Cryptococcus luteolusAntarctic soilVictoria Landdi Menna (1966b), Atlas et al. (1978)
Cryptococcus nyarrowiiAntarctic soil; snow samplesDry Valleys, South Victoria Land; Vestfold Hills, Ingrid Christensen CoastThomas-Hall & Watson (2002), Connell et al. (2008)
Cryptococcus skinneriDecaying woodRoss Island, Ross Sea BayArenz et al. (2006)
Cryptococcus tephrensisDecaying woodRoss Island, Ross Sea BayArenz et al. (2006)
Cryptococcus victoriaeAntarctic soil; decaying woodBotany Bay, South Victoria Land; Ross Island, Ross Sea Bay; Vestfold Hills, Ingrid Christensen CoastMontes et al. (1999), Thomas-Hall et al. (2002), Arenz et al. (2006)
Cryptococcus vishniaciiCryptococcus lupi; Cryptococcus consortionis, Cryptococcus socialisAntarctic soil; decaying woodDry Valleys, South Victoria Land; Ross Desert, South Victoria Land; Ross Island, Ross Sea BayVishniac & Hempfling (1979a), Baharaeen & Vishniac (1982), Vishniac (1985b), Arenz et al. (2006), Connell et al. (2008)
Cryptococcus watticusSnow and Antarctic soilVestfold Hills, Ingrid Christensen CoastGuffogg et al. (1998)
Cryptococcus wieringaeDecaying woodRoss Island, Ross Sea BayArenz et al. (2006)
Cystofilobasidium infirmominiatumAccretion iceVostok Research StationD'Elia et al. (2005)
Cystofilobasidium maceransRhodotorula maceransAntarctic soilRoss Dependencydi Menna (1966b)
Dioszegia antarcticaAntarctic soilDry Valleys, South Victoria LandConnell et al. (2008)
Dioszegia cryoxericaAntarctic soilDry Valleys, South Victoria LandConnell et al. (2008)
Dioszegia hungaricaCryptococcus hungaricusDecaying woodRoss Island, Ross Sea BayArenz et al. (2006)
Dioszegia statzelliaeCryptococcus statzelliaeAntarctic soilVestfold Hills, Ingrid Christensen CoastThomas-Hall et al. (2002)
Glaciozyma martiniiSead spongeVestfold Hills, Ingrid Christensen Coast; Dry Valleys, South Victoria LandTurchetti et al. (2011)
Glaciozyma watsoniiAntarctic soilVestfold Hills, Ingrid Christensen Coast; Dry Valleys, South Victoria LandTurchetti et al. (2011)
Glaciozyma antarcticaLeucosporidium antarcticumAntarctic soil; seawater; subglacial waterAdmiralty Bay, King George Island; South Victoria LandTurkiewicz et al. (2003, 2005), Turchetti et al. (2011)
Guehomyces pullulansTrichosporon pullulansAntarctic soilVictoria Landdi Menna (1966b)
Leucosporidum scottiiCandida scottiiAlgal sample; Antarctic soilDry Valleys, South Victoria Land; South Victoria Landdi Menna (1966b), Goto et al. (1969), Atlas et al. (1978)
Malassezia restrictaAntarctic soil; decaying woodAlexander Island, Antarctic Peninsula; Ross Island, Ross Sea BayArenz et al. (2006), Bridge & Newsham (2009)
Mrakia blollopisAntarctic soilVestfold Hills, Ingrid Christensen CoastThomas-Hall et al. (2010)
Mrakia frigidaCandida frigida, Candida nivalisAntarctic soilVictoria Landdi Menna (1966a, b)
Mrakia gelidaCandida gelida; Mrakia stokesiiAntarctic soilDry Valleys, South Victoria Landdi Menna (1966a, b), Connell et al. (2008)
Mrakia psychrophilaAntarctic soilFildes Peninsula, Antarctic PeninsulaXin & Zhou (2007)
Mrakia robertiiAntarctic soilVestfold Hills, Ingrid Christensen CoastThomas-Hall et al. (2010)
Mrakiella niccombsiiAntarctic soilVestfold Hills, Ingrid Christensen CoastThomas-Hall et al. (2010)
Pseudozyma antarcticaCandida antarctica; Sporobolomyces antarcticusAntarctic soil; lake sedimentArena Valley, South Victoria Land; Dry Valleys, South Victoria LandGoto et al. (1969), Atlas et al. (1978)
Rhodosporidium kratochvilovaeAntarctic soilDry Valleys, South Victoria LandConnell et al. (2008)
Rhodosporidium sphaerocarpumAntarctic marine samplesAntarctic OceanNewell & Fell (1970)
Rhodotorula aurantiacaUnknownAntarctic Station Dumont d'Urville, Adélie LandAlchihab et al. (2009)
Rhodotorula auriculariaeCandida auriculariaeAntarctic soilSchirmacher Oasis, Queen Maud LandRay et al. (1992)
Rhodotorula diffluensCandida diffluensLake sedimentDry Valleys, South Victoria LandGoto et al. (1969)
Rhodotorula glutinisAntarctic soil; ice cores; lake waterDry Valleys, South Victoria Land; Vostok Research Stationdi Menna (1966b), Goto et al. (1969), Abyzov (1993)
Rhodotorula graminisAntarctic soilDry Valleys, South Victoria Landdi Menna (1966b), Cameron (1971)
Rhodotorula ingeniosaCandida ingeniosaAntarctic soilSchirmacher Oasis, Queen Maud LandRay et al. (1992)
Rhodotorula laryngisAntarctic soil; decaying woodDry Valleys, South Victoria Land; Ross Island, Ross Sea BayArenz et al. (2006), Connell et al. (2008)
Rhodotorula marinaAntarctic soilVictoria Landdi Menna (1966b)
Rhodotorula minutaRhodotorula texensisAntarctic soil; lake water; moulting feathers of penguinsDry Valleys, South Victoria Land; Livingston Island, Antarctic Peninsula; McMurdo Station, Ross Island, Ross Sea Baydi Menna (1966b), Goto et al. 1969), Cameron (1971), Atlas et al. (1978), Pavlova et al. (2009)
Rhodotorula mucilaginosaRhodotorula rubraAccretion ice; Antarctic soil; decaying wood; lake waterDry Valleys, South Victoria Land; Ross Island, Ross Sea Bay; Schirmacher Oasis, Queen Maud Land; Vostok Research Station; West Ongul Island, Lutzow-Holm Baydi Menna (1966b), Goto et al. (1969), Cameron (1971), Atlas et al. (1978), Baublis et al. (1991), Ray et al. (1992), Arenz et al. (2006), Connell et al. (2008), D'Elia et al. (2005), Pavlova et al. (2009)
Rhodotorula pallidaAntarctic soilVictoria Landdi Menna (1966b)
Sporidiobolus johnsoniiSporobolomyces holsaticusAntarctic soilDry Valleys, South Victoria LandVishniac & Hempfling (1979a)
Sporidiobolus metaroseusSporobolomyces roseusAntarctic soilDry Valleys, South Victoria LandVishniac & Hempfling (1979a)
Sporidiobolus salmonicolorSporobolomyces salmonicolorAntarctic soil; decaying wood; lichen; moss samplesBrown Peninsula, Ross Ice Shelf; Livingston Island, Antarctic Peninsula; Ross Island, Ross Sea BayAtlas et al. (1978), Arenz et al. (2006), Poli et al. (2010)
Sporobolomyces symmetricusDecaying woodRoss Island, Ross Sea BayArenz et al. (2006)
Trichosporon cutaneumUnknownShowa Base, Est Ongul Island, Lutzow-Holm BaySoneda (1961)
Trichosporon moniliiformeTrichosporon cutaneum var. antarcticumLake waterDry Valleys, South Victoria LandGoto et al. (1969)
Yeast-like organisms
Aureobasidium pullulansAntarctic soilBrown Peninsula, Ross Ice Shelf; Dry Valleys, South Victoria Land; Vostok Research StationAtlas et al. (1978), Baublis et al. (1991), D'Elia et al. (2005)
  • Species identified using culture-dependent and/or culture-independent approaches.

Some historical Antarctic sampling campaigns are undoubtedly noteworthy for their ecological implications. Soils, water and other biological samples collected from Victoria Land were extensively investigated (di Menna, 1966a, b; Goto et al., 1969; Vishniac & Hempfling, 1979a, b; Baharaeen & Vishniac, 1982; Vishniac, 1985a, b; Baublis et al., 1991; Vishniac & Kurtzman, 1992; Montes et al., 1999; Connell et al., 2008, 2010). di Menna (1966a, b) investigated yeast diversity of soils sampled at Victoria Land (Table 1). Yeast abundance varied from 5 to over 105 CFU g−1. Surprisingly, di Menna found no correlation between yeast distribution and pH. Yeasts isolated by other authors were identified as belonging to both ascomycetous and basidiomycetous species: the genera Candida, Cryptococcus, Dioszegia and Rhodotorula were most commonly represented (Table 1). Variations of seasonal temperature, the sporadic availability of liquid water, and changes of some chemical and physical features (e.g. pH and electrical conductivity) apparently affected yeast distribution (Vishniac, 2006b).

Other Antarctic regions were considered. Davis Station is a permanent station managed by the Australian Antarctic Division located near the Vestfold Hills. Some Australian scientists (Thomas-Hall & Watson, 2002; Thomas-Hall et al., 2002, 2010; Guffogg et al., 2004) reported novel species belonging to the genera Cryptococcus, Dioszegia, Mrakia and Mrakiella (Table 1) in soil, snow and other organic material. Additionally, Scorzetti et al. (2000) and Alchihab et al. (2009) identified a few strains isolated from Adélie Land (the portion of the Antarctic coast between 136° and 142°E) as representing Cryptococcus adeliensis and Rhodotorula aurantiaca (Table 1).

The Antarctic Peninsula is the northernmost ice-covered part of the Antarctic mainland: its ecosystem is currently under study to monitor the effects of climate change. Yeasts belonging to the genera Cryptococcus, Mrakia, Leucosporidium and Sporobolomyces (Table 1) have quite recently been isolated from soil, moss and lichen (Pavlova et al., 2002, 2009; Turkiewicz et al., 2003, 2005; Poli et al., 2010).

Some scientific stations are in central Antarctica: due to their harsh climatic conditions, sampling campaigns carried out near these stations are considered to be of paramount ecological interest. The Amundsen–Scott South Pole United States Antarctic station is located at the geographic South Pole. Pioneer ecological studies were carried out there by Jacobs & Shafer (1964), who found strains of Candida parapsilosis from upwind snow and ice cores. Vostok is a Russian (former Soviet) Antarctic station located at the center of the East Antarctic Ice Sheet. Abyzov (1993) and D'Elia et al. (2009) carried out studies on accretion ice sections and ancient ice cores (from 3000–7000 to about 1 000 000–2 000 000 years old) drilled in proximity to the station: The authors identified isolates as belonging to species of the genera Cryptococcus, Cystofilobasidium, Rhodotorula and Pseudozyma (Table 1).

Recent investigations have combined both culture-dependent and culture-independent approaches. An interesting study was performed on the diversity of yeasts and filamentous fungi in old wood structures and surrounding soils of Ross Island, a volcanic island in the Ross Sea. This was the site of three historic expeditions carried out by early explorers to the South Pole (Robert F. Scott and Ernest Shackleton). The presence of both ascomycetous and basidiomycetous yeast species (genera Debaryomyces, Dipodascus, Bulleromyces, Cryptococcus, Dioszegia, Rhodotorula, Sporidiobolus and Sporobolomyces) (Table 1) was found by using a combined approach (isolation and denaturing gradient gel electrophoresis) (Arenz et al., 2006). By contrast, Bridge & Newsham (2009) used PCR amplification of internal transcribed spacer regions 1 and 2 and cloning to determine the diversity of yeasts and filamentous fungi in soils from Mars Oasis (Alexander Island, Antarctic Peninsula). Basidiomycetous yeasts and filamentous fungi made up 22% of the clone sequences obtained: three yeast sequences were successfully assigned to Candida intermedia and Malassezia restricta (Table 1).

Psychrophilic yeasts in the Arctic region

The Arctic is a vast, ice-covered ocean and permafrost area, which can be approximately defined as north of the Arctic Circle (66°33′N): it includes the Arctic Ocean and parts of Canada, Russia, Greenland, the United States, Norway, Sweden, Finland and Iceland. Like Antarctica, the Arctic cryosphere harbors psychrophilic yeast life. The list of yeast species isolated from this area is summarized in Table 2. Forty-six species (eight ascomycetes and 38 basidiomycetes) and A. pullulans were found (Table 2). As in Antarctica, about one-third belonged to the genus Cryptococcus. Ice-related habitats and soil (including permafrost) were the most common source of isolates. A partial habitat-dependent distribution was observed (Table 2).

View this table:

List of yeast species isolated from Arctic: original taxonomic designations reported in the literature were updated according to the latest taxonomic guidelines (Kurtzman et al., 2011)

SpeciesOriginal taxonomic designationIsolation sourceLocalityReference(s)
Ascomycetous yeasts
Candida parapsilosisBrine puddles on sea-ice surfaceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2011)
Candida rugosaArctic soilEast Greenlanddi Menna (1966b)
Debariomyces maramusSeawaterKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2011)
Debaryomyces hanseniiCryopegs of permafrost; seawater, sub-glacial iceSiberian sea coast, Russia tundra zone near the East Siberian Sea coast; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayGilichinsky et al. (1997), Butinar et al. (2011)
Metschnikowia bicuspidataSeawaterKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2011)
Metschnikowia zobelliiPuddles on snow/iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2011)
Meyerozyma guilliermondiiPichia guilliermondiiCryopegs of permafrost; seawater, sub-glacial iceSiberian sea coast, Russia tundra zone near the East Siberian Sea coast; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayGilichinsky et al. (1997), Butinar et al. (2011)
Protomyces inouyeiIce in a glacier caveKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2011)
Basidiomycetous yeasts
Bulleromyces albusGlacier surface iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus adeliensisGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus albidosimilisGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus albidusArctic soil; glacier basal ice; ice coresGreenland; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, Norwaydi Menna (1966b), Ma et al. (2006), Butinar et al. (2007)
Cryptococcus carnescensGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus diffluensArctic soilEast Greenlanddi Menna (1966b)
Cryptococcus gastricusSmall puddles near to meltwater stream from glaciersKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayPathan et al. (2010)
Cryptococcus gilvescensGlacier surface iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus heimaeyensisSoilHeimaey, Vestmannaeyar, IcelandVishniac (2002)
Cryptococcus laurentiiArctic soil; cryopegs of permafrost; glacier basal iceEast Greenland; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, Norway; Siberian sea coast, Russia tundra zone near the East Siberian Sea coastdi Menna (1966b), Gilichinsky et al. (1997), Butinar et al. (2007)
Cryptococcus liquefaciensGlacier surface and basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007, 2011)
Cryptococcus magnusGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus oeirensisGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus saitoiGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Cryptococcus tephrensisSoilVestmannaeyar, IcelandVishniac (2002)
Cryptococcus terricolaCryptococcus terricolusSmall puddles near to meltwater stream from glaciersKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayPathan et al. (2010)
Cryptococcus victoriaeCryopegs of permafrost; glacier surface and basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, Norway; Siberian sea coast, Russia tundra zone near the East Siberian Sea coastGilichinsky et al. (1997), Butinar et al. (2007)
Cystofilobasidium capitatumCystofilobasidium lari-mariniFrozen soilSeltjarnarnes, IcelandBirgisson et al. (2003)
Cystofilobasidium maceransCryptococcus maceransFrozen soil; glacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, Norway; Seltjarnarnes, IcelandBirgisson et al. (2003), Butinar et al. (2007)
Filobasidium uniguttulatumCryptococcus uniguttulatusGlacier basal ice; ice coresGreenland; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayMa et al. (2006), Butinar et al. (2007)
Guehomyces pullulansTrichosporon pullulansArctic soilEast Greenlanddi Menna (1966b)
Leucosporidiella creatinivoraRhodotorula creatinivoraPermafrost soilEastern-Siberian ArcticGolubev (1974)
Leucosporidiella fragariaGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Leucosporidiella muscorumRhodotorula muscorumSmall puddles near to meltwater stream from glaciersKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayPathan et al. (2010)
Leucosporidiella yakuticaRhodotorula yakuticaPermafrost soilEastern-Siberian ArcticGolubev (1974)
Leucosporidum scottiiCandida scottiiArctic soilEast Greenlanddi Menna (1966b)
Mrakia gelidaCandida gelidaArctic soil; small puddles near to meltwater stream from glaciersEast Greenland; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, Norwaydi Menna (1966b), Pathan et al. (2010)
Mrakia psychrophilaSmall puddles near to meltwater stream from glaciersKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayPathan et al. (2010)
Mrakiella aquaticaCryptococcus aquaticusFrozen soilHeidmörk, IcelandBirgisson et al. (2003)
Mrakiella cryoconitiSedimentGydan peninsula, North Siberia, RussiaGounot (1986), Margesin & Fell (1999)
Rhodosporidium diobovatumGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Rhodotorula arcticaSandProvideniya, Komsomolskaya Bay, Beringia, RussiaVishniac (2006b), Vishniac & Takashima (2010)
Rhodotorula glacialisSmall puddles near to meltwater stream from glaciersKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayPathan et al. (2010)
Rhodotorula glutinisArctic soilEast Greenlanddi Menna (1966b)
Rhodotorula laryngisGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Rhodotorula minutaArctic soil; glacier basal iceEast Greenland; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, Norwaydi Menna (1966b), Butinar et al. (2007)
Rhodotorula mucilaginosaRhodotorula rubraGlacier surface and basal ice; ice coresGreenland; Kongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayMa et al. (2006), Butinar et al. (2007, 2011)
Trichosporon mucoidesGlacier basal iceKongsfjorden fjord, Spitsbergen, Svalbard archipelago, NorwayButinar et al. (2007)
Yeast-like organisms
Aureobasidium pullulansCryopegs of permafrostSiberian sea coast, Russia tundra zone near the East Siberian Sea coastGilichinsky et al. (1997)
  • Species identified using culture-dependent and/or culture-independent approaches.

Due to their easier accessibility, only a few Arctic areas were considered: the Svalbard archipelago, north-east Siberia, Greenland and Iceland. The Svalbard archipelago is located midway between Norway and the North Pole. Recently, a number of basidiomycetous yeast species (genera Bulleromyces, Cryptococcus, Cystofilobasidium, Filobasidium, Leucosporidiella, Mrakia, Rhodosporidium, Rhodotorula and Trichosporon) were found in some glacier-associated habitats (Table 2) (Butinar et al., 2007; Lee et al., 2010; Pathan et al., 2010). The alternative use of media of low water activity revealed a higher incidence of halophilic ascomycetous yeasts (Butinar et al., 2011).

Siberia is an extensive and harsh region including almost all of northern Asia (comprising the central and eastern portion of the Russian Federation). Psychrophilic yeasts have sporadically been isolated from Siberian permafrost. A few authors found significant numbers of viable ascomycetous and basidiomycetous yeasts, and yeast-like organisms (Table 2) in permafrost layers with an estimated age from 100 000 to 3 million years (Dmitriev et al., 1997; Golubev, 1998; Gilichinsky et al., 2005). More recent studies found the presence of two novel species (Mrakiella cryoconiti and Rhodotorula arctica) in Siberian sediments and sand (Margesin & Fell, 2008; Vishniac & Takashima, 2010).

Greenland and Iceland are located between the Arctic and Atlantic Ocean. The weight of the massive Greenland ice sheet has depressed the central land area to form a basin lying about 300 m below sea level. The ice flows generally to the coast from the center of the island. By contrast, Iceland consists of a plateau characterized by sand fields, mountains and glaciers, while many glacial rivers flow to the sea through the lowlands. Vishniac (2002) and Birgisson et al. (2003) reported the presence of species of the genera Cryptococcus and Cystofilobasidium (Table 2) in Iceland soils. A combined culture-dependent and culture-independent approach was applied for investigating yeast diversity of ancient Greenland ice cores (up to 140 000 years old). Both yeast isolates and DNA sequences revealed a noticeable yeast diversity (Table 2). The authors postulated that some yeasts could remain viable for over 100 000 years entrapped in ice (Ma et al., 1999).

Psychrophilic yeasts in Asian and Himalayan regions

Unlike other glacial areas, yeast diversity of the Asian cryosphere (excluding Siberia) has been considered only sporadically. Shivaji et al. (2008) isolated psychrophilic yeasts from the soil surrounding Roopkund Lake, Himalayas (India). Strains were identified as belonging to Cryptococcus gastricus and to a novel species, Rhodotorula himalayensis. Likewise, Uetake et al. (2011) used both culture-dependent and culture-independent approaches to detect yeast abundance (over 104 CFU mL−1) in snow and ice cores of the high-altitude Belukha glacier (Altay Mountains, along the border between Russia and Kazakhstan). 26S rRNA clonal analysis directly amplified (after melting) from ice cores revealed the presence of strains of the genus Rhodotorula. Based on the analysis of peaks in yeast concentration, the role of occasional surface melting could be one of the factors influencing yeast propagation from surface to deep snow layers.

Psychrophilic yeasts in European glaciers

European glaciers have recently been studied as reservoirs of psychrophilic yeast life. The non-Arctic European cryosphere is essentially comprises the Alps, Apennines and Pyrenees. The complete list of yeast species isolated from European glacier-associated habitats is summarized in Table 3. Overall, 41 species (one ascomycete and 40 basidiomycetes) were found: Cryptococcus was the main genus represented (about 39% of the total species). Yeast-like organisms (A. pullulans and Exophiala dermatitidis) were also observed (Table 3).

View this table:

List of yeast species isolated from European glaciers: original taxonomic designations reported in the literature were updated according to the latest taxonomic guidelines (Kurtzman et al., 2011)

SpeciesOriginal taxonomic designationIsolation sourceLocalityReference(s)
Ascomycetous yeasts
Candida santamariaeSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Basidiomycetous yeasts
Cryptococcus adeliensisSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus aeriusSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus albidosimilisSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus dimennaeSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus festucosusSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus gastricusSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus gilvescensSediments, ice and melwater stream from glaciersForni and Sforsellina glaciers, Italian AlpsTurchetti et al. (2008)
Cryptococcus oeirensisSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus saitoiNaganishia globosaSediments and ice from glaciersCalderone glacier, Apennines, Italy; Forni and Sforsellina glaciers, Italian AlpsTurchetti et al. (2008), Branda et al. (2010)
Cryptococcus stepposusSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus tephrensisSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus terreusSoil and sedimentsBrenner pass, AustriaBergauer et al. (2005)
Cryptococcus terricolaCryptococcus terricolusSediments from glaciers; soilBrenner pass, Austria; Forni and Sforsellina glaciers, Italian AlpsBergauer et al. (2005), Turchetti et al. (2008)
Cryptococcus victoriaeSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus watticusSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cryptococcus wieringaeSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cystofilobasidium capitatumSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Cystofilobasidium maceransCryptococcus maceransSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Dioszegia croceaSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Erythrobasidium hasegawianumSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Glaciozyma martiniiSediments from glaciersCalderone glacier, Apennines, ItalyTurchetti et al. (2011)
Glaciozyma watsoniiSediments from glaciersForni and Sforsellina glaciers, Italian AlpsTurchetti et al. (2011)
Guehomyces pullulansSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Laucosporidiella creatinivoraRhodotorula creatinivoraSediments from glaciers; soilBrenner pass, Austria; Forni and Sforsellina glaciers, Italian AlpsBergauer et al. (2005), Turchetti et al. (2008)
Mastigobasidium intermediumSediments from glaciers; soilBrenner pass, Austria; Calderone glacier, Apennines, ItalyBergauer et al. (2005), Branda et al. (2010)
Mrakia blollopisSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Mrakia frigidaGlacier cryoconitesAlpine glacier, AustriaMargesin et al. (2009)
Mrakia gelidaSediments and meltwater stream from glaciersCalderone glacier, Apennines, Italy; Forni and Sforsellina glaciers, Italian AlpsTurchetti et al. (2008), Branda et al. (2010)
Mrakia robertiiSediments and meltwater stream from glaciersForni and Sforsellina glaciers, Italian AlpsThomas-Hall et al. (2010)
Mrakiella aquaticaCryptococcus aquaticusFrozen soil; sediments from glaciersCalderone glacier, Apennines, Italy; Heidmörk, IcelandBirgisson et al. (2003), Branda et al. (2010)
Mrakiella cryoconitiGlacier cryoconites; sediments from glaciersCalderone glacier, Apennines, Italy; Stubaier glacier, Tyrol, AustriaMargesin & Fell (1999), Branda et al. (2010)
Rhodosporidium lusitaniaeSoil and sedimentsBrenner pass, AustriaBergauer et al. (2005)
Rhodotorula bacarumSediments from glaciersForni and Sforsellina glaciers, Italian AlpsTurchetti et al. (2008)
Rhodotorula colostriSediments from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)
Rhodotorula glacialisGlacier cryoconites; mud at glacier foot; sediments and ice from glaciersForni and Sforsellina glaciers, Italian Alps; Stubaier glacier, Tyrol, AustriaMargesin et al. (2007a, b), Turchetti et al. (2008)
Rhodotorula ingeniosaSoil and sedimentsBrenner pass, AustriaBergauer et al. (2005)
Rhodotorula laryngisSediments and ice from glaciersCalderone glacier, Apennines, Italy; Forni and Sforsellina glaciers, Italian AlpsTurchetti et al. (2008), Branda et al. (2010)
Rhodotorula psychrophenolicaGlacier cryoconites; mud at glacier foot; sediments from glaciersCalderone glacier, Apennines, Italy; Forni and Sforsellina glaciers, Italian Alps; Stubaier glacier, Tyrol, AustriaMargesin et al. (2007a, b), Turchetti et al. (2008), Branda et al. (2010)
Rhodotorula psychrophilaSoil and sedimentsBrenner pass, AustriaMargesin et al. (2011, b)
Sporidiobolus metaroseusSporobolomyces roseusSediments from glaciers; soilBrenner pass, Austria; Calderone glacier, Apennines, ItalyBergauer et al. (2005), Branda et al. (2010)
Yeast-like organisms
Aureobasidium pullulansGranitic sediments from glaciers; sediments and meltwater stream from glaciersCalderone glacier, Apennines, Italy; Damma glacier, central Swiss Alps; Forni and Sforsellina glaciers, Italian AlpsTurchetti et al. (2008), Branda et al. (2010), Brunner et al. (2011)
Exophiala dermatitidisSediments and meltwater stream from glaciersCalderone glacier, Apennines, ItalyBranda et al. (2010)

The Alps are one of the great mountain complexes of Europe: the highest mountain in Europe is Mont Blanc (4810 m a.s.l.) on the Italian–French border. Austrian, Italian and Swiss groups have studied the diversity of psychrophilic yeasts in both polluted and non-polluted Alpine habitats. The presence of a number of basidiomycetous species (genera Cryptococcus, Glaciozyma, Leucosporidiella, Mastigobasidium, Mrakia, Mrakiella, Rhodosporidium, Rhodotorula and Sporobolomyces) was observed (Table 3) (Bergauer et al., 2005; Krallish et al., 2006; Turchetti et al., 2008; Brunner et al., 2011). Yeast abundance up to 105 CFU g−1 of supra- and subglacial sediment was observed. Cryptococcus gilvescens accounted for over 50% of the total strains in Italian Alpine glaciers (Turchetti et al., 2008). A handful of novel species were described for the first time (Table 3) (Margesin et al., 2007a, b; Margesin & Fell, 2008; Thomas-Hall et al., 2010; Turchetti et al., 2011).

With the disappearance of the Corral de la Veleta Glacier (Sierra Nevada, Spain) in 1913, the Calderone Glacier (Apennines, Italy) became the southernmost European glacier: yeast abundance up to 103 CFU g−1 was observed. Isolates were identified as belonging to a number of ascomycetous and basidiomycetous species (Table 3). Cryptococcus gastricus accounted for about 40% of the total isolates (Branda et al., 2010).

To our knowledge, no combined culture-dependent and culture-independent approaches have been used in the South European cryosphere.

Psychrophilic yeasts in South American glaciers

Like other glacial ecosystems, the South American cryosphere harbors psychrophilic yeast life. All ecological studies have been carried out in the area of Nahuel Huapi National Park, Patagonia, Argentina. Yeast species isolated from South American glacier-associated habitats are listed in Table 4. Forty-one species (four ascomycetes and 37 basidiomycetes) were found: about one-third belong to the genus Cryptococcus. Meltwater running off from glaciers was the source of all strains (Table 4). Argentinean scientists studied yeast diversity in aquatic environments nearby glaciers: yeast abundance was up to 103 CFU L−1. Cryptococcus victoriae, Leucosporidiella fragaria and Rhodotorula mucilaginosa were the most frequent species (Libkind et al., 2003; de Garcia et al., 2007; Brandão et al., 2011) (Table 4). The novel species Cryptococcus spencermartinsiae, Cystofilobasidium lacus-mascardii and Wickerhamomyces patagonicus were described (de García et al., 2010a, b; Libkind et al., 2009). No combined culture-dependent and culture-independent approaches were used.

View this table:

List of yeast species isolated from South American glacier-associated habitats: original taxonomic designations reported in the literature were updated according to the latest taxonomic guidelines (Kurtzman et al., 2011)

SpeciesOriginal taxonomic designationIsolation source and localityReference(s)
Ascomycetous yeasts
Candida parapsilosisWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Candida sakèWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Debaryomyces hanseniiCandida famataWater from lakes of glacial origin; Nahuel Huapi National Parkde Garcia et al. (2007), Brandão et al. (2011)
Wickerhamomyces patagonicusMeltwater stream from glaciers; Castaño Overo Riverde Garcia et al. (2010a)
Basidiomycetous yeasts
Bullera dendrophilaWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus adeliensisWater from lakes of glacial origin; Nahuel Huapi National Parkde Garcia et al. (2007), Brandão et al. (2011)
Cryptococcus cylindricusMeltwater stream from glaciers, Frias riverde Garcia et al. (2007)
Cryptococcus diffluensWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus festucosusMeltwater stream from glaciers, Garganta del Diablo river; water from lakes and lagoon of glacial origin; Nahuel Huapi National Parkde Garcia et al. (2007), Brandão et al. (2011)
Cryptococcus heveanensisWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus laurentiiMeltwater stream from glaciers, Garganta del Diablo and Castaño Overo river; lagoon of glacial origin, Ventisquero Negrode Garcia et al. (2007)
Cryptococcus magnusWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus saitoiWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus spencermartinsiaeMeltwater stream from glaciers; Frias glacier at Mount Tronadorde García et al. (2010a, b)
Cryptococcus stepposusWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus tephrensisWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus victoriaeWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cryptococcus wieringaeWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Cystofilobasidium capitatumWater from lakes and lagoons of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008), Brandão et al. (2011)
Cystofilobasidium infirmominiatumWater from lakes and lagoons of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008), Brandão et al. (2011)
Cystofilobasidium lacus-mascardiiWater of glacial origin; Mascardi lakeLibkind et al. (2009)
Cystofilobasidium maceransCryptococcus maceransLagoon of glacial origin, Ventisquero Negrode Garcia et al. (2007)
Dioszegia croceaMeltwater stream from glaciers, Frias riverde Garcia et al. (2007)
Dioszegia fristingensisMeltwater stream from glaciers, Frias riverde Garcia et al. (2007)
Dioszegia hungaricaMeltwater stream from glaciers, Frias river; water of glacial origin; Nahuel Huapi lakede Garcia et al. (2007), Brandão et al. (2011)
Guehomyces pullulansWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Leucosporidiella creatinivoraMeltwater stream from glaciers, Frias riverde Garcia et al. (2007)
Laucosporidiella fragariaMeltwater stream from glaciersde Garcia et al. (2007)
Mrakia frigidaMeltwater stream from glaciers, Garganta del Diablode Garcia et al. (2007)
Rhodosporidium babjevaeWater from lakes and lagoons of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008)
Rhodosporiodium diobovatumWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Rhodosporidium kratochvilovaeWater from lakes and lagoons of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008), de Garcia et al. (2007)
Rhodotorula colostriMeltwater stream from glaciers, Frias river; water from lakes and lagoons of glacial origin, Nahuel Huapi National Parkde Garcia et al. (2007), Brandão et al. (2011)
Rhodotorula laringisWater from lakes and lagoons of glacial origin, Nahuel Huapi National Parkde Garcia et al. (2007), Brandão et al. (2011)
Rhodotorula minutaWater from lakes of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008)
Rhodotorula mucilaginosaWater from lakes and lagoons of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008), de Garcia et al. (2007), Brandão et al. (2011)
Rhodotorula pinicolaWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)
Sporidiobolus metaroseusSporobolomyces roseusWater from lakes of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008)
Sporidiobolus salmonicolorSporobolomyces salmonicolorWater from lakes of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008)
Sporobolomyces ruberrimusWater from lakes and lagoons of glacial origin, Nahuel Huapi National ParkLibkind et al. (2008), de Garcia et al. (2007)
Udeniomyces pannonicusMeltwater stream from glaciers, Frias riverde Garcia et al. (2007)
Yeast-like organisms
Aureobasidium pullulansWater of glacial origin; Nahuel Huapi lakeBrandão et al. (2011)

Adaptation strategies of psychrophilic yeasts to cold

Cold adaptation requires a complex range of structural and functional adaptations. Low (or even sub-zero) temperatures influence the life of all organisms in multiple ways: reduced growth rates, increased medium viscosity, reduced membrane fluidity, altered protein conformation and decreased nutrient availability (Margesin et al., 2007a, b; Poindexter, 2009). Psychrophilic microorganisms (including yeasts) sharing natural environments are subjected to seasonal or permanent cold conditions. Hence, they evolved a number of adaptation strategies: (1) increase of membrane fluidity at low temperatures (by changing the composition of fatty acids); (2) synthesis of protecting proteins as a response to thermal stresses; (3) synthesis of cryoprotectant macromolecules for reducing the presence of cytoplasm ice crystals; (4) subcellular, molecular and metabolic changes; (5) reduction of growth rates; and (6) synthesis of cold-active enzymes. The list of adaptation strategies adopted by psychrophilic yeasts to overcome cold conditions is summarized in Table 5.

View this table:

List of adaptation strategies of psychrophilic yeasts to cold conditions

Physiological featureSignificance on yeast cell biologySpeciesOriginal taxonomic designationReference(s)
Changes of composition of membrane lipids
Increased percentage of unsaturated fatty acidsIncreased fluid state of cell membrane at subzero temperaturesCryptococcus gastricus; Cryptococcus gilvescens; Cryptococcus terricola; Leucosporidiella creatinivora; Leucosporidiella muscorum; Leucosporidum scottii; Mrakia frigida; Mrakia psychrophila; Rhodotorula glacialis; Rhodotorula laryngisCandida scottii; Cryptococcus terricolus; Leucosporidium frigidum; Leucosporidium gelidum; Leucosporidium nivalis; Rhodotorula creatinivora; Rhodotorula muscorumKates & Baxter (1964), Arthur & Watson (1976), Watson et al. (1976), Turkiewicz et al. (2005), Rossi et al. (2009), Pathan et al. (2010)
Synthesis of protecting proteins (csps and hsps)
Production of cold shock proteins (csps)Adaptation to life at subzero temperaturesTrichosporon pullulansJulseth & Inniss (2010)
Production of heat shock proteins (hsps) upon exposure to mild (nonlethal) heat shockPossible role in inducing moderate thermnotoleranceCandida psychrophila; Guehomyces pullulans; Leucosporidium fellii; Leucosporidium scottii; Mrakia frigida; Mrakia gelida; Sporobolomyces salmonicolorTrichosporon pullulans; Mrakia stokesiiBerg et al. (1987),Deegenaars & Watson (1997, 1998), Julseth & Inniss (1990b)
Synthesis of cryoprotectant macromolecules
Production of extracellular ice-binding glycoproteinsIncreased freeze–thaw survival of cellsLeucosporidium sp.Lee et al. (1962)
Subcellular, metabolic and molecular changes
Production of atypical anucleate budsEvent associated with DNA replicationMrakia gelidaLeucosporidium stokesiiSilver et al. (1977)
Increased activity of key enzymes of EMP pathway and TCA cycle at low temperatureActive cell metabolism at low temperaturesNot specifiedXin & Zhou (2000)
Increased amino acid incorporation at sub-zero temperatureActive cell metabolism at subzero temperatures; offset and repair of macromolecular occurring after prolonged entrapment in frozen materialsCryptococcus adeliensis; Cryptococcus vistoriae; Rhodotorula glutinisAmato et al. (2009)
Reduction of growth kinetic parameters
Reduced growth rate and increased biomass production at low temperatureAdvantage in ologotrophic habitatsCryptococcus gilvescens; Leucosporidiella creatinivora; Rhodotorula aurantiaca; Rhodotorula glacialis, Rhodotorula laryngisRhodotorula creatinivoraSabri et al. (2000),Margesin (2003), Rossi et al. (2009)
Synthesis of cold-active enzymes
Synthesis of cold-active enzymesActive cell metabolism at low temperaturesCryptococcus adeliensis, Cryptococcus albidus; Cryptococcus aquaticus; Cryptococcus gastricus; Cryptococcus laurentii; Cryptococcus macerans, Cryptococcus terricola; Cystofilobasidium capitatum; Dioszegia crocea; Leucosporidiella creatinivora; Leucosporidiella fragaria; Leucosporidiella muscorum; Leucosporidium antarcticum; Mrakia frigida; Mrakia gelida, Mrakia psychrophila; Rhodotorula glacialis; Rhodotorula mucilaginosa; Sporobolomyces ruberrimusCryptococcus adeliae, Cryptococcus terricolus; Cystofilobasidium lari-marini; Rhodotorula muscorumAmoresano et al. (2000), Gomes et al. (2000), Petrescu et al. (2000), Scorzetti et al. (2000), Nakagawa et al. (2002), Pavlova et al. (2002), Birgisson et al. (2003), Margesin et al. (2010), Turkiewicz et al. (2005), Brizzio et al. (2007), Pathan et al. (2010)
Synthesis of miscellaneous compounds
Synthesis of cold-active killer proteinsCompetitive advantage in ologotrophic habitatsMrakia frigidaHua et al. (2004)

Changes in the composition of membrane lipids

A number of studies have clarified that the ability to adjust membrane fluidity by regulating the synthesis of fatty acids is crucial for cold adaptation. Important alterations in membrane lipid composition of psychrophilic yeasts were detected some time ago: in particular, increased fatty acid unsaturation, decreased fatty acid average chain length and decreased sterol/phospholipid ratio (Inniss, 1975; Margesin & Miteva, 2011). Among the three, the increase of unsaturation degree is the most studied mechanism (Russell, 2008). Generally, an increase of fatty acid unsaturated bonds allows continued membrane fluidity even at subzero temperatures (Watson, 1984; Vishniac, 2006a). Eukaryotic microorganisms (including yeasts) exhibit some Δ6, Δ9, Δ12 and Δ15 desaturases, which are responsible for the synthesis of polyunsaturated fatty acids by repetitive desaturation to give characteristic products, such as linoleic acid or linolenic acid (Russell, 2008). Extremely low temperature increases the percentage of unsaturated fatty acids (from 50% to 90% of the total) in membranes of psychrophilic yeasts (McMurrough & Rose, 1973; Arthur & Watson, 1976; Watson, 1984; Chintalapati et al., 2004; Pathan et al., 2010). In particular, at low and subzero temperatures, linolenic (35–50%) and linoleic (25–30%) acids predominated in the fatty acid profiles of species of the genera Mrakia, Leucosporidium and Rhodotorula. By contrast, at temperatures close to the maximum for growth, oleic (20–40%) and linoleic (30–50%) acids were the major components (Watson et al., 1976; Moat et al., 2002; Rossi et al., 2009).

Synthesis of response proteins (csps and hsps)

Both prokaryotes and eukaryotes exhibit cold-shock responses upon a rapid temperature downshift. The regulatory molecular processes and configuration of the proteins involved have been studied. Yeasts currently synthesize cold-shock proteins (csps) to overcome the deleterious effects of cold-shock on cell viability. Although the production of csps has been observed since the 1990s in mesophilic yeasts (e.g. Saccharomyces cerevisiae) (Phadtare et al., 1999; Phadtare & Inouye, 2008), only a few authors have reported the ability of psychrophilic yeasts to synthesize csps (Julseth & Inniss, 1990a). On the other hand, psychrophilic yeasts also synthesize heat-shock proteins (hsps) as a defense mechanism against an increase of temperature (heat-shock). Both types of studies increased the basic knowledge about the ability of psychrophilic yeasts to acquire either cold-resistance or moderate thermotolerance (> 20 °C) and could be a key ecological feature increasing their ability to colonize either permanently or temporarily cold environments (Deegenaars & Watson, 1997, 1998; Margesin et al., 2007a, b). Guehomyces pullulans (former Trichosporon pullulans) was subjected to a series of increasing cold-shocks to test its ability to synthesize csps: two-dimensional electrophoresis revealed a different csp pattern depending on the temperature range. Cells grown above their optimal growth temperature reduced their ability to induce the synthesis of csps. This suggests that the cold-shock range could influence the type of csps produced by psychrophilic yeasts (Julseth & Inniss, 1990a). On the other hand, heat shock resulted in an increase in thermotolerance (Julseth & Inniss, 1990b). Other hsps produced by psychrophilic yeasts were isolated and characterized (Berg et al., 1987; Deegenaars & Watson, 1997). Interestingly, induced thermotolerance was seldom coincident with hsp synthesis and trehalose accumulation (Deegenaars & Watson, 1998).

Synthesis of cryoprotectant macromolecules

It is well known that a low freezing rate can damage the cytoplasm membrane (Kawahara, 2008). Hence, the synthesis of cryoprotectant (antifreeze) molecules is essential to reduce the cell damage that occurs in natural habitats, where freezing rates are quite low. Among them, trehalose biosynthesis pathways are widely distributed in nature as cell protection against osmotic stress (Kandror et al., 2002). High cytoplasm concentrations of trehalose were observed in Mrakia frigida and Leucosporidium fellii as a strategy to reduce the freezing point of the intracellular fluid (Deegenaars & Watson, 1997, 1998). Moreover, Pan et al. (2005) reported that trehalose stabilizes a cold-active protease by preventing its autolysis.

Other cryoprotectant mechanisms have been observed in psychrophilic yeasts. Lee et al. (2010) reported the ability of an Arctic Leucosporidium sp. strain to secrete a glycosylated ice-binding protein (IBP). The IBP exhibited thermal hysteresis and recrystallization inhibition activities. The full-length cDNA for IBP was determined: it encoded a 261-amino-acid protein with molecular weight of 26.8 kDa (including a N-terminal signal peptide and one potential N-glycosylation site). The deduced protein showed high sequence identity with other IBPs from fungi, diatoms and bacteria, and clustered with a class of ice-active proteins (Lee et al., 2010).

Molecular and metabolic changes and reduction of growth kinetic parameters

Molecular and metabolic events that occur as responses to growth at different temperature were observed in some psychrophilic yeasts. The subcellular morphology of Mrakia gelida (former Leucosporidium stokesii) was investigated under permissive (15 and 20 °C) and restrictive (23 and 25 °C) temperatures: nuclear staining revealed that buds formed at 23 °C were anucleate as the consequence of temperature-sensitive inhibition of DNA synthesis. The cessation of growth at temperatures above 20 °C could be due to the inability to complete DNA synthesis and normal cell division cycle (Silver et al., 1977; Silver & Sinclair, 1979).

Metabolic changes observed in yeasts grown at extremely low temperatures were considered. Xin & Zhou (2000) checked both the activity and the stability of some key enzymes of the EMP (Embden–Meyerhof–Parnas) pathway and TCA (tricarboxylic acid) cycle both in psychrophilic and in mesophilic yeasts: enzymes produced by the former exhibited higher activity at low temperature and weak thermal stability. The ability of psychrophilic yeasts to remain metabolically active under subzero temperatures was recently underlined by Amato et al. (2009). Frozen cells of Antarctic basidiomycetous yeasts showed a metabolism (assessed by measuring rates of [3H]leucine incorporation into the acid-insoluble macromolecular fraction) apparently directed towards maintenance and survival, but not growth. Under these conditions, cells may be capable of offsetting and repairing the macromolecular damage occurring after prolonged entrapment in frozen materials.

The thermal dependence of growth kinetic parameters of psychrophilic and mesophilic yeasts has recently been investigated. Overall, a clear dichotomy was observed: the temperature at which microbial growth was fastest was generally different from the temperature allowing the production of the highest amount of yeast biomass. In some cases, the origin of strains affected the temperatures allowing the maximum growth rate (Sabri et al., 2000; Margesin, 2009; Rossi et al., 2009).

Synthesis of cold-active enzymes

The synthesis of cold-active enzymes (psychrophilic enzymes) is probably one of the most investigated adaptation strategies to low temperatures (Gerday et al., 1997). The increased activity of cold-active enzymes at low temperatures is based on their improved structural flexibility, including a possible modification of the active site (Gerday et al., 1997; Feller & Gerday, 2003). The enhanced plasticity of cold-active enzymes is often considered to be responsible for their weak thermal stability. This is due to their adaptation to cold conditions, which gave rise to molecular structures with increased sensitivity towards various denaturing agents. This suggests a direct link between activity and stability of cold-active enzymes (i.e. maintenance of activity at low temperatures requires the weakening of intramolecular forces, which results in reduced stability) (Feller & Gerday, 2003).

Due to their increasing biotechnological relevance, a detailed description of the synthesis of cold-active enzymes by some psychrophilic yeast species is reported below.

Biotechnological potential of psychrophilic yeasts

Due to their distinctive ability to grow and metabolize at low temperatures, psychrophilic yeasts are attracting academic and industrial attention for their huge biotechnological potential. However, despite the plethora of studies so far published, only a few molecules produced by those organisms are currently on the market (Margesin & Feller, 2010). However, a number of other possible products are still confined to the laboratory and will eventually be developed into profitable ventures. The list of biotechnological features of psychrophilic yeasts is summarized in Table 6.

View this table:

List of biotechnological properties of psychrophilic yeasts

PropertiesBiotechnological potentialSpeciesOriginal taxonomic designationReference(s)
Production of cold-active enzymes
Production of α-amylases and glucoamylasesFood and beverage processing industryPseudozyma antarcticaCandida antarcticaDe Mot & Verachtert (1987)
Production of aspartyl proteinasesConversion of substrates via biocatalysisCandida humicolaCryptococcus humicolaRay et al. (1992)
Production of β-fructosidases and α-glucosidasesFood and beverage processing industryLeucosporidium antarcticumTurkiewicz et al. (2005)
Production of β-glucosidasesHydrolysis of cellulose-containing materialsCryptococcus albidusPavlova et al. (2002)
Production of lipases and proteasesFood and beverage processing industryCryptococcus laurentii; Cryptococcus macerans; Dioszegia crocea; Leucosporidiella creatinivora; Leucosporidiella fragaria; Pseudozyma antarctica; Rhodotorula colostri; Rhodotorula mucilaginosa; Sporobolomyces ruberrimusCandida antarcticade Maria et al. (2005), Brizzio et al. (2007), Brandão et al. (2011)
Production of pectate lyasesLow-temperature pretreatment of wastewatersMrakia frigidaMargesin et al. (2005)
Production of polygalacturonasesFruit and vegetable processing industryCryptococcus aquaticus; Cryptococcus macerans; Cystofilobasidium capitatumCystofilobasidium lari-mariniBirgisson et al. (2003)
Production of xylanasesXylan hydrolysis for biofuel and solvent industryCryptococcus adeliensis; Cryptococcus albidusCryptococcus adeliaeAmoresano et al. (2000), Gomes et al. (2000), Petrescu et al. (2000), Scorzetti et al. (2000)
Production of serine proteinasesConversion of substrates via biocatalysisLeucosporidium antarcticumPazgier et al. (2003), Turkiewicz et al. (2003)
Degradation of pollutant compounds at low temperature
Degradation of phenol-related compounds at low temperatureBioremediation strategies of cold polluted environmentsCryptococcus terreus; Cryptococcus terricola; Rhodotorula creatinivora; Sporidiobolus metaroseusSporidiobolus metaroseusBergauer et al. (2005), Krallish et al. (2006)
Production of other miscellaneous compounds
Production of γ-decalactone at low temperaturesAroma compounds for foods and beveragesRhodotorula aurantiacaAlchihab et al. (2009)
Production of exopolysaccharides (EPS)Biopolymers for pharmaceutical, food and cosmetic industryCryptococcus flavus; Sporobolomyces salmonicolorPavlova et al. (2009), Poli et al. (2010)
Production of extracellular yeast glycoproteins (YGs)Investigation on the effect of YGs on cold-stored rat liversLeucosporidium antarcticumTilšer et al. (1996)
Production of intracellular lipidsProduction of biodiesel via transesterificationRhodotorula glacialisAmaretti et al. (2010)

Production of cold-active enzymes

Studies on the production of cold-active enzymes from psychrophilic yeasts have been mainly devoted to the search for detergent additives (e.g. lipases) for ecofriendly cold water washing, cellulases for textile and biofuel processing, and enzymes for the food industry (Sproessler, 1993; Gerday et al., 1997; Feller & Gerday, 2003). They might provide significant advantages in terms of: (1) potential economic benefits in biocatalysis through energy savings and (2) transformation of heat-sensitive products and easy inactivation at moderate temperature after catalytic treatment (Gerday et al., 1997; Feller & Gerday, 2003). Lipases A and B are lipases produced by Pseudozyma antarctica (former Candida antarctica), probably the unique example of patented cold-active enzymes from psychrophilic yeasts (De Maria et al., 2005). Lipase B is at present sold as Novozym 435 by Novozymes (Denmark) (Margesin & Feller, 2010), whereas Lipase A exhibits a higher thermal stability (≤ 90 °C) than other lipases (De Maria et al., 2005).

Other hydrolases have been studied, although the scientific and analytic level of the studies was extremely variable: some authors used fine enzyme purification and characterization protocols, whereas others simply checked the crude activity of cell-free extracts. Two amylases produced by Ps. antarctica (former Ca. antarctica) were purified to homogeneity: the α-amylase was active on cyclodextrins, whereas glucoamylase exhibited high debranching activity (De Mot & Verachtert, 1987). By contrast, Ray et al. (1992) found that an Antarctic Cryptococcus humicola (former Candida humicola) secreted an extracellular aspartyl protease (molecular mass = 36 kDa). Interestingly, this extracellular cold-active protease was active at temperatures ranging from 0 to 45 °C, with an optimum activity at 37 °C.

As underlined by Shivaji & Prasad (2009), cold-active xylanases may be used for digestion of agricultural, industrial or sewage wastes at low temperatures. A glycosylated xylanase (338 amino acids) produced by an Antarctic Cryptococcus albidus strain was structurally elucidated. MS analysis revealed the occurrence of N-glycosylation only at Asn254, which was modified by high-mannose structure (Amoresano et al., 2000). Likewise, Petrescu et al. (2000) studied a cold-active glycosylated xylanase produced by an Antarctic strain of Cr. adeliensis (former Cryptococcus adeliae). The xylanase exhibited 84% identity and lower thermostability than its homologue synthesized by Cr. albidus. The cold-active xylanase exhibited a higher catalytic efficiency between 0 to 20 °C: computerized analysis of molecular models indicated that the cold adaptation consists of discrete changes in the three-dimensional structure.

An extracellular serine proteinase synthesized by an Antarctic Glaciozyma antarctica (former Leucosporidium antarcticum) strain was characterized. The sequence of 35 N-terminal amino acid residues of the proteinase showed 31% homology to that of proteinase K (Pazgier et al., 2003). Likewise, Turkiewicz et al. (2003) characterized a glycosylated serine proteinase (molecular mass = 34.4 kDa) secreted by a strain of the same species. The enzyme exhibited low optimal temperature (25 °C), poor thermal stability and high catalytic efficiency from 0 to 25 °C.

There has been increasing industrial interest in large-scale screening surveys for selecting psychrophilic yeasts as a source of novel cold-active enzymes. Different cell-free enzymatic profiles (amylase, protease, esterase, pectinase, chitinase and cellulase activity) were observed dependent on the species and origin of the strains (Margesin et al., 2003; Brizzio et al., 2007; Pathan et al., 2010; Brandão et al., 2011). The influence of culture conditions (e.g. pH, temperature) on the activity and stability of some cold-active enzymes (α-glucosidases, β-glucosidases, β-fructosidases, pectate lyases, xylanases) synthesized by psychrophilic yeasts was also investigated (Gomes et al., 2000; Pavlova et al., 2002; Margesin et al., 2005; Turkiewicz et al., 2005).

Degradation of pollutant compounds at low temperature

The ability of psychrophilic yeasts to degrade efficiently a wide range of phenol-related compounds and petroleum hydrocarbons at low temperatures is another important character of biotechnological relevance. A few excellent reviews have been recently published (Margesin, 2007; Margesin & Feller, 2010).

Yeasts isolated from polluted glacial habitats degraded representative fractions of petroleum hydrocarbons at 10 °C: about 30% of strains assimilated phenol, phenanthrene or anthracene. All phenol-degrading strains expressed catechol 1,2-dioxygenase activities (Margesin et al., 2003). Likewise, Bergauer et al. (2005) screened a set of psychrophilic yeasts isolated from Alpine habitats for their ability to degrade phenol and phenol-related monoaromatic compounds at 10 °C: the ability to assimilate some non- or low volatile aromatic compounds was a strain-related feature. More recently, it has been that psychrophilic basidiomycetous yeasts fully degraded up to 12.5–15 mM phenol at 10 °C under fed-batch cultivation. Immobilization may improve phenol degradation by yeast cells (Krallish et al., 2006; Margesin & Feller, 2010).

Production of other miscellaneous compounds

A number of recent studies carried out at the laboratory scale have demonstrated that psychrophilic yeasts are able to produce other miscellaneous compounds of industrial interest. Alchihab et al. (2009) studied the synthesis of γ-decalactone by an Antarctic Rh. aurantiaca strain at low temperature. Highest production (6.6 g L−1) was obtained in a fermenter settled at 14 °C by using a medium containing 20 g L−1 castor oil. On the other hand, Antarctic Cryptococcus flavus strains were found to produce extracellular polysaccharides (EPs). Highest production (5.75 g L−1) was obtained at 24 °C. The composition of the EPs (molecular mass = 1.01 MDa) was established: 55.1% mannose, 26.1% glucose, 9.6% xylose and 1.9% galactose (Pavlova et al., 2009). Likewise, Poli et al. (2010) studied the Antarctic yeast Sporidiobolus salmonicolor (former Sporobolomyces salmonicolor) as a source of high-molecular-mass mannan-like EPs: maximum yield (5.64 g L−1) was achieved at 22 °C.

Due to their ability to be successfully used to produce biodiesel (by catalyzed trans-esterification with short-chain alcohols) microbial lipids has garnered increasing interest. Some psychrophilic yeasts isolated from the Alpine cryosphere were recently found to accumulate high amounts of intracellular lipids (20–70% of biomass) between −3 and 20 °C (Rossi et al., 2009; Amaretti et al., 2010).

Outstanding issues and future prospects

Despite the overabundance of published literature, some crucial questions remain to be answered. And the factors determining the distribution of psychrophilic yeasts in the worldwide cryosphere remain to be identified. A critical point could be the great diversity of isolation procedures used in over 60 years of investigations. As recently underlined by Shivaji & Prasad (2009), most Antarctic studies were carried our using very different (and even unsuitable) protocols (e.g. incubation temperatures that were too high or too low, incubation time too short, media exhibiting too low pH, too low osmotic pressure, etc.). This could explain, with some exceptions, the apparently random distribution of most psychrophilic yeasts in glacial habitats (di Menna, 1960, 1966a; Vishniac, 2006a; Shivaji & Prasad, 2009).

By comparing the list of yeast species isolated from the worldwide cryosphere, more than 120 different species (20 ascomycetes, 102 basidiomycetes and two yeast-like organisms) were found: overall, about one-third belonged to the genus Cryptococcus (Tables 1)–4). Aureobasidium pullulans, Cr. adeliensis, Cryptococcus tephrensis, Cr. Victoriae and Cystofilobasidium macerans are currently widespread over glacial and nonglacial habitats (Kurtzman et al., 2011). By contrast, other species have been isolated exclusively from a well-defined geographical area: Candida psychrophila, Cryptococcus antarcticus, Cryptococcus friedmannii, Cryptococcus nyarrowii, Dioszegia antarctica, Dioszegia cryoxerica, Dioszegia statzelliae, Glaciozyma antarctica and Mrakiella niccombsii from Antarctica, Leucosporidiella yakutica and Rh. arctica from the Arctic, Rhodotorula psychrophenolica and Rhodotorula psychrophila from European glaciers, and Cyst. lacus-mascardii from the South American cryosphere (Tables 14). On the other hand, Rh. himalayensis has been isolated solely the from Himalayas (Shivaji et al., 2008). Several questions seem pertinent. Are these species endemic? What factors apparently control the occurrence of psychrophilic yeasts in glacial habitats globally? Why do basidiomycetes generally predominate?

Vishniac (1999, 2006a) underlined that, given its remoteness and isolation from other landmass for millions of years, Antarctica should be amongst the first places to look for endemic organisms. However, Vishniac also stressed that the simple evidence that a few species have been isolated exclusively from a given geographic area does not constitute sufficient evidence supporting endemism because the possibility that these species may in the future be found in other glacial habitats cannot be excluded. A few species (e.g. Ps. antarctica, Cr. victoriae) were first isolated from Antarctica (Goto et al., 1969; Montes et al., 1999) (Table 1), but later were identified from other nonglacial habitats (Vishniac, 1999; Kurtzman et al., 2011).

With reference to the factors apparently controlling the global occurrence of psychrophilic yeasts in the cryosphere, Vishniac (2006b) carried out an exhaustive latitudinal gradient multivariate analysis to explore the relationships between characteristics of habitats and the distribution of yeast taxa in soil communities and to verify what factors (if any) affected global yeast distribution. Although the study included both glacial and nonglacial habitats, Vishniac concluded that combinations of a few physical and chemical characters (temperature, rain and snowfall, electrical conductivity, etc.) could explain over 40% of the distribution of the predominant yeast species.

The apparent prevalence of basidiomycetes in the worldwide cryosphere has generally been confirmed, although this evidence has been questioned (Butinar et al., 2011). It could reflect the effect of a more efficient adaptation of this taxon to the selective pressure typical of glacial ecosystems (e.g. formation in some cases of a polysaccharide capsule) (Vishniac, 2006a; Shivaji & Prasad, 2009). Margesin & Miteva (2011) have underlined that capsular Cryptococcus species and the related genus Mrakia dominate in Antarctic desert soils. Nevertheless, it is reasonable to assume that supplementary (hitherto undiscovered) adaptation strategies could favor basidiomycetous yeasts in cryosphere ecosystems.

Another criticism potentially confusing the ecological picture of yeast diversity in the global cryosphere is the lack of studies combining both culture-dependent and culture-independent approaches. This is undoubtedly a problem, because in certain cases nonculturable strains may be very abundant. As underlined by Margesin & Miteva (2011), culture-independent studies could reveal a wider range of diversity in the worldwide cryosphere in the future. Moreover, a significant part of the current literature lacks sufficient information about the chemical, physical and ecological conditions of sampling sites. Accordingly, the existing literature represents at best a partial picture of the yeast diversity occurring in worldwide glacial habitats.

A significant number of well-established insights about the adaptation strategies of psychrophilic yeasts to the severe conditions typical of the cryosphere have been published since the 1960s. Among them, the production of unsaturated fatty acids, csps and hsps, and cold-adapted enzymes represents the most well studied. However, some recent discoveries (e.g. the synthesis of intracellular IBPs) certainly represent a further evolution towards a deeper understanding of the mechanisms leading to both survival and growth of psychrophilic yeasts in glacial ecosystems.

The successful biotechnological use of psychrophilic yeasts is also one of the challenges of the 21st century. However, a number of issues should be addressed to ensure the stable (and profitable) use of psychrophilic yeasts: (1) enrichment of the number of strains conserved ex-situ in culture collections by funding new sampling campaigns in the worldwide cryosphere, (2) carrying out large-scale screening surveys for selecting novel hyperproducing strains, and (3) development of new and efficient processes for the production of molecules of commercial interest at low temperatures. In this background, given the retreat of the global cryosphere due to ongoing climate change (Benn & Evans, 1998; Nesje & Dahl, 2000; Zemp et al., 2006), long-term ex-situ conservation of psychrophilic microorganisms (considered to be in danger of extinction) may acquire increasing scientific interest in light of their incomparable biotechnological value.

Footnotes

  • Editor: Nina Gunde-Cimerman

References

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