Skip to main content
SpringerLink
Log in

Yeasts in high Arctic glaciers: the discovery of a new habitat for eukaryotic microorganisms

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Recently a new habitat for microbial life has been discovered at the base of polythermal glaciers. In ice from these subglacial environments so far only non-photosynthetic bacterial communities were discovered, but no eukaryotic microorganisms. We found high numbers of yeast cells, amounting to a maximum of 4,000 CFU ml−1 of melt ice, in four different high Arctic glaciers. Twenty-two distinct species were isolated, including two new yeast species. Basidiomycetes predominated, among which Cryptococcus liquefaciens was the dominant species (ca. 90% of total). Other frequently occurring species were Cryptococcus albidus, Cryptococcus magnus, Cryptococcus saitoi and Rhodotorula mucilaginosa. The dominant yeast species were psychrotolerant, halotolerant, freeze-thaw resistant, unable to form mycelium, relatively small-sized and able to utilize a wide range of carbon and nitrogen sources. This is the first report on the presence of yeast populations in subglacial ice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abyzov SS (1993) Microorganisms in the Antarctic ice. In: Friedmann EI (ed) Antarctic microbiology. Wiley-Liss, New York

    Google Scholar 

  • Babjeva I, Reshetova I (1998) Yeast resources in natural habitats at polar circle latitude. Food Technol Biotechnol 36:1–5

    Google Scholar 

  • Blomberg A, Adler L (1992) Physiology of osmotolerance in fungi. Adv Microb Physiol 33:145–212

    PubMed  CAS  Google Scholar 

  • Blomberg A (2000) Metabolic surprises in Saccharomyces cerevisiae during adaptation to saline conditions: questions, some answers and a model. FEMS Microbiol Lett 182:1–8

    Article  PubMed  CAS  Google Scholar 

  • Botha A, Wolfaardt GM (2000) Yeast biofilms: an unexplored natural phenomenon. In: Abstracts of the 10th international symposium on yeasts. Arnhem, The Netherlands, 27th August–1st September 2000

  • Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N (2005) Yeast diversity in hypersaline habitats. FEMS Microbiol Lett 244:229–234

    Article  PubMed  CAS  Google Scholar 

  • Christner BC (2002) Incorporation of DNA and protein precursors into macromolecules by bacteria at −15°C. Appl Environ Microbiol 68:6435–6438

    Article  PubMed  CAS  Google Scholar 

  • Christner BC, Mosley-Thompson E, Thompson LG, Zagorodnov V, Sandman K, Reeve JN (2000) Recovery and identification of viable bacteria immured in glacial ice. Icarus 144:479–485

    Article  Google Scholar 

  • Dmitriev VV, Gilichinsky DA, Faizutdinova RN, Shershunov IN, Golubev WI, Duda VI (1997) Occurrence of viable yeasts in 3-million-year-old permafrost in Siberia. Mikrobiologiya 66:655–660

    Google Scholar 

  • Ekström G, Nettles M, Abers GA (2003) Glacial earthquakes. Science 302:622–624

    Article  PubMed  CAS  Google Scholar 

  • Fahnestock M (2003) Glacial flow goes seismic. Science 302:578–579

    Article  PubMed  CAS  Google Scholar 

  • Faizutdinova RN, Suzina NE, Duda VI, Petrovskaya LE, Gilichinsky DA (2005) Yeasts isolated from ancient permafrost. In: Castello JD, Rogers SO (eds) Life in ancient ice. Princeton University Press, Princeton and Oxford

    Google Scholar 

  • Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50:1351–1371

    PubMed  CAS  Google Scholar 

  • Foght J, Aislabie J, Turner S, Brown CE, Ryburn J, Saul DJ, Lawson W (2004) Culturable bacteria in subglacial sediments and ice from two southern hemisphere glaciers. Microb Ecol 47:329–340

    Article  PubMed  CAS  Google Scholar 

  • Fonseca A (1992) Utilization of tartaric acid and related compounds by yeasts: taxonomic implications. Can J Microbiol 38:1242–1251

    Article  PubMed  CAS  Google Scholar 

  • Fonseca A, Scorzetti G, Fell JW (2000) Diversity in the yeast Cryptococcus albidus and related species as revealed by ribosomal DNA sequence analysis. Can J Microbiol 46:7–27

    Article  PubMed  CAS  Google Scholar 

  • Gadanho M, Almeida JM, Sampaio JP (2003) Assessment of yeast diversity in a marine environment in the south of Portugal by microsatellite-primed PCR. Anton Leeuw Int J G 84:217–227

    Article  CAS  Google Scholar 

  • Gaidos E, Lanoil B, Thorsteinsson T, Graham A, Skidmore M, Han SK, Rust T, Popp B (2004) A viable microbial community in a subglacial volcanic crater lake, Iceland. Astrobiology 4:327–344

    Article  PubMed  CAS  Google Scholar 

  • Gunde-Cimerman N, Zalar P, de Hoog GS, Plemenitaš A (2000) Hypersaline water in salterns – natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240

    CAS  Google Scholar 

  • Gunde-Cimerman N, Sonjak S, Zalar P, Frisvad JC, Diderichsen B, Plemenitaš A (2003) Extremophilic fungi in Arctic ice: a relationship between adaptation to low temperature and water activity. Phys Chem Earth 28:1273–1278

    Google Scholar 

  • Gunde-Cimerman N, Butinar L, Sonjak S, Turk M, Uršič V, Zalar P, Plemenitaš A (2005) Halotolerant and halophilic fungi from coastal environmnt in the Arctics. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Arcahea, Bacteria and Eucarya. Springer, Dordrecht

    Google Scholar 

  • Ito H, Koduh S (1997) Characteristics of water in Kongsfjorden, Svalbard. Proc NIPR Symp Polar Meteorol Glaciol 11:221–232

    Google Scholar 

  • Ivanushkina NE, Kochkina GA, Ozerskaya SM (2005) Fungi in ancient permafrost sediments of the Arctic and Antarctic regions. In: Castello JD, Rogers SO (eds) Life in ancient ice. Princeton University Press, Princeton and Oxford

    Google Scholar 

  • Jones GEB (1976) Recent advances in aquatic mycology. The Gresham Press, Old Woking, Surrey

    Google Scholar 

  • Knight PG (1997) The basal ice layer of glaciers and ice sheets. Quat Sci Rev 16:975–993

    Article  Google Scholar 

  • Krebs CJ (1999) Ecological methodology. Addison Wesley Longman, Menlo Park

    Google Scholar 

  • Kurtzman CP, Fell JW (1998) The yeasts: a taxonomic study. Elsevier, Amsterdam

    Google Scholar 

  • Lahav R, Fareleira P, Nejidat A, Abeliovich A (2002) The identification and characterisation of osmotolerant yeast isolates from chemical wastewater evaporation ponds. Microb Ecol 43:338–396

    Article  CAS  Google Scholar 

  • Libkind D, Brizzio S, van Broock M (2004) Rhodotorula mucilaginosa, a carotenoid producing yeast strain from a Patagonian high-altitude lake. Folia Microbiol 49:19–25

    Article  CAS  Google Scholar 

  • Libkind D, Brizzio S, Ruffini A, Gadanho M, van Broock M, Sampaio JP (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Anton Leeuw Int J G 84:313–322

    Article  CAS  Google Scholar 

  • Ma LJ, Catranis CM, Starmer WT, Rogers SO (1999) Revival and characterization of fungi from ancient polar ice. Mycologist 13:70–73

    Article  Google Scholar 

  • Ma LJ, Rogers SO, Catranis CM, Starmer WT (2000) Detection and characterization of ancient fungi entrapped in glacial ice. Mycologia 92:286–295

    Google Scholar 

  • Ma LJ, Catranis CM, Starmer WT, Rogers SO (2005) The significance and implications of the discovery of filamentous fungi in glacial ice. In: Castello JD, Rogers SO (eds) Life in ancient ice. Princeton University Press, Princeton and Oxford

    Google Scholar 

  • Middelhoven WJ (1997) Identity and biodegradative abilities of yeasts isolated from plants growing in arid climate. Anton Leeuw Int J G 72:81–89

    Article  CAS  Google Scholar 

  • Nagahama T, Hammamoto M, Nakase T, Takami H, Horikoshi K (2001) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. Anton Leeuw Int J G 80:101–110

    Article  CAS  Google Scholar 

  • Onofri S, Selbmann L, Zucconi L, Pagano S (2004) Antarctic microfungi as models for exobiology. Planet Space Sci 52:229–237

    Article  Google Scholar 

  • Pennisi E (2003) Neither cold nor snow stops tundra fungi. Science 301:1307

    Article  PubMed  CAS  Google Scholar 

  • Poglazova MN, Mitskevich IN, Abyzov SS, Ivanov MV (2001) Microbiological characterization of the accreted ice of subglacial Lake Vostok, Antarctica. Mikrobiologiia 70:838–846

    Google Scholar 

  • Reeve JN, Christner BC, Kvitko BH, Mosley-Thompson E, Thompson LG (2002) Life in glacial ice. In: Abstracts of the 4th international congress on extremophiles. Naples, Italy, 22th–26th September 2002

  • Sampaio JP (1999) Utilization of low molecular weight aromatic compounds by heterobasidiomycetous yeasts: taxonomic implications. Can J Microbiol 45:491–512

    Article  PubMed  CAS  Google Scholar 

  • Sampaio JP, Gadanho M, Bauer R, Weiss M (2003) Taxonomic studies in the Microbotryomycetidae: Leucosporidium golubevii sp. nov., Leucosporidiella gen. nov. and the new orders Leucosporidiales and Sporidiobolales. Mycol Prog 2:53–68

    Article  Google Scholar 

  • Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361

    Article  PubMed  CAS  Google Scholar 

  • Scorzetti G, Fell JW, Fonseca A, Statzell-Tallman A (2002) Systematics of basidiomycetous yeasts: a comparison of large subunit D1/D2 and internal transcribed spacer rDNA regions. FEMS Yeast Res 2:495–517

    PubMed  CAS  Google Scholar 

  • Skidmore ML, Foght JM, Sharp MJ (2000) Microbial life beneath a high Arctic glacier. Appl Environ Microbiol 66:3214–3220

    Article  PubMed  CAS  Google Scholar 

  • Starmer WT, Fell YW, Catranis CM, Aberdeen V, Ma LJ, Zhou S, Rogers SO (2005) Yeasts in the genus Rhodotorula recovered from the Greenland ice sheet. In: Castello JD, Rogers SO (eds) Life in ancient ice. Princeton University Press, Princeton and Oxford

    Google Scholar 

  • Takashima M, Sugita T, Shinoda T, Nakase T (2003) Three new combinations from the Cryptococcus laurentii complex: Cryptococcus aureus, Cryptococcus carnescens and Cryptococcus peneaus. Int J Syst Evol Microbiol 53:1187–1194

    Article  PubMed  CAS  Google Scholar 

  • Tosil S, Casado B, Gerdol R, Caretta G (2002) Fungi isolated from Antarctic mosses. Polar Biol 25:262–268

    Google Scholar 

  • van Uden N (1984) Temperature profiles of yeasts. Adv Microb Physiol 25:195–251

    PubMed  Google Scholar 

  • Vishniac HS (1987) Psychrophily and the systematics of yeast-like fungi. In: de Hoog GS, Smith MT, Weijman ACM (eds) Proceedings of an international symposium on the perspectives of taxonomy, ecology and phylogeny of yeasts and yeast-like fungi. CBS, Delft; Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • Vishniac HS (2002) Cryptococcus tephrensis, sp. nov., and Cryptococcus heimaeyensis, sp. nov.; new anamorphic basidiomycetous yeast species from Iceland. Can J Microbiol 48:463–467

    Article  PubMed  CAS  Google Scholar 

  • Vishniac HS, Klinger J (1986) Extreme environments. Yeasts in the Antarctic deserts. In: Megušar F, Gantar M (eds) Perspectives in microbial ecology. Slovene Society for Microbiology, Ljubljana

    Google Scholar 

  • Vishniac HS, Onofri S (2002) Cryptococcus antarcticus var. circumpolaris var. nov., a basidiomycetous yeast from Antarctica. Anton Leeuw Int J G 83:231–233

    Article  Google Scholar 

  • Yarrow D (1998) Methods for the isolation, maintenance and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts: a taxonomic study. Elsevier Science Publishers, Amsterdam

    Google Scholar 

Download references

Acknowledgements

The work in Kongsfjorden was funded by EU Large Scale Facility Fund. The work on identification of yeasts was supported by the Slovenian Ministry of Education, Science and Sport and Slovenia—Portugal bilateral collaboration. Special thanks are due to Nick Cox (NERC Station) for his logistic support and to Martin Grube for help with sequencing of yeasts.

Author information

Authors and Affiliations

  1. Laboratory of Biotechnology, National Institute of Chemistry, Hajdrihova 19, SI-1001, Ljubljana, Slovenia

    Lorena Butinar & Nina Gunde-Cimerman

  2. Centro de Recursos Microbiológicos (CREM), Biotechnology Unit, Faculty of Sciences and Technology, New University of Lisbon, 2829-516, Caparica, Portugal

    Isabel Spencer-Martins

  3. Biology Department, Biotechnical Faculty, University of Ljubljana, Večna pot 111, SI-1000, Ljubljana, Slovenia

    Nina Gunde-Cimerman

Authors
  1. Lorena Butinar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabel Spencer-Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nina Gunde-Cimerman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lorena Butinar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Butinar, L., Spencer-Martins, I. & Gunde-Cimerman, N. Yeasts in high Arctic glaciers: the discovery of a new habitat for eukaryotic microorganisms. Antonie van Leeuwenhoek 91, 277–289 (2007). https://doi.org/10.1007/s10482-006-9117-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-006-9117-3

Keywords

Search

Navigation