, 15:573 | Cite as

Psychrophilic yeasts from Antarctica and European glaciers: description of Glaciozyma gen. nov., Glaciozyma martinii sp. nov. and Glaciozyma watsonii sp. nov.

  • Benedetta TurchettiEmail author
  • Skye R. Thomas Hall
  • Laurie B. Connell
  • Eva Branda
  • Pietro Buzzini
  • Bart Theelen
  • Wally H. Müller
  • Teun Boekhout
Original Paper


Field campaigns in Antarctica, Greenland and the Italian glaciers aiming to explore the biodiversity of these disappearing environments identified several undescribed yeast strains unable to grow at temperature above 20°C and belonging to unknown species. Fourteen of these strains were selected and grouped based on their morphological and physiological characteristics. Sequences of the D1/D2 and ITS regions of the ribosomal RNA demonstrated that the strains belong to unknown species related to Leucosporidium antarcticum. The new genus Glaciozyma is proposed and two new species are described, namely Glaciozyma martinii sp. nov. and Glaciozyma watsonii sp. nov. Additionally, re-classification of Leucosporidium antarcticum as Glaciozyma antarctica is proposed. Strains of Glaciozyma form a monophyletic clade and a well separated lineage within class Microbotryomycetes (Pucciniomycotina, Basidiomycota). The description of Glaciozyma genus and the re-classification of L. antarcticum reduce the polyphyletic nature of the genus Leucosporidium.


Glaciozyma gen. nov. Glaciozyma martinii sp. nov. Glaciozyma watsonii sp. nov. Psychrophilic yeasts Antarctica European glaciers Cold-adapted biodiversity 



This work was supported by the SYNTHESYS Project ( which is financed by the European Community Research Infrastructure Action under the FP6 “Structuring the European Research Area” Programme, by FEMS (Federation of European Microbiological Societies) and by MIUR (PRIN projects 2009). We thank Raytheon Polar Support Service, UNAVCO, and PHI for logistical and laboratory support while in Antarctica. Partial funding was provided for this project by the US NSF Office of Polar Programs to L. B. Connell (OPP-0125611). The use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the US Department of Interior or the US Geological Survey of any product or service to the exclusion of others that may be suitable.

Supplementary material

792_2011_388_MOESM1_ESM.tif (575 kb)
Fig. S1 Phylogeny of the Glaciozyma clade including the representative strains of the related species K. eriophori and C. hydrophilum. Maximum parsimony tree of D1/D2 region of LSU rRNA sequences. The topology was rooted with Rh. minuta. Bootstrap percentages from 100 replications shown on the branches (value below 50% are not shown). GenBank accession numbers of the sequences are indicated after strain numbers. (TIFF 574 kb)
792_2011_388_MOESM2_ESM.tif (568 kb)
Fig. S2 Phylogeny of the Glaciozyma clade including the representative strains of the related species K. eriophori. Maximum parsimony tree of ITS regions including 5.8 gene of the rDNA sequences. The topology was rooted with Rh. minuta. Bootstrap percentages from 100 replications shown on the branches (value below 50% are not shown). GenBank accession numbers of the sequences are indicated after strain numbers. (TIFF 568 kb)


  1. Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH, Piepenbring M, McLaughlin DJ, Szabo LJ, Begerow D, Sampaio JP, Bauer R, Weiss M, Oberwinkler F, Hibbett D (2006) An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 98(6):896–905PubMedCrossRefGoogle Scholar
  2. Bab’eva IP, Lisichkina GA (2000) A new species of psychrophilic basidiomycetous yeasts Leucosporidium fasciculatum sp. nov. Mikrobiologiya 69:801–804Google Scholar
  3. Bauer R, Oberwinkler F, Vanky K (1997) Ultrastructural markers and systematics in smut fungi and allied taxa. Can J Bot 75:1237–1314CrossRefGoogle Scholar
  4. Bauer R, Begerow D, Sampaio JP, Weiss M, Oberwinkler F (2006) The simple-septate basidiomycetes: a synopsis. Mycol Prog 5:41–66CrossRefGoogle Scholar
  5. Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369PubMedCrossRefGoogle Scholar
  6. Connell LB, Redman R, Craig S, Scorzetti G, Iszard M, Rodriguez R (2008) Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microb Ecol 56(3):448–459PubMedCrossRefGoogle Scholar
  7. Connell LB, Redman R, Rodriguez R, Barrett A, Iszard M, Fonseca A (2010) Dioszegia antarctica sp nov. and Dioszegia cryoxerica sp. nov., psychrophilic basidiomycetous yeasts from polar desert soils in Antarctica. Int J Syst Evol Microbiol 60(6):1466–1472PubMedCrossRefGoogle Scholar
  8. de Garcia V, Brizzio S, Libkind D, Rosa CA, van Broock M (2010) Wickerhamomyces patagonicus sp. nov., an ascomycetous yeast species from Patagonia, Argentina. Int J Syst Evol Microbiol 60:1693–1696PubMedCrossRefGoogle Scholar
  9. Deming JW (2002) Psychrophiles and polar regions. Curr Opin Microbiol 5:301–309PubMedCrossRefGoogle Scholar
  10. Doubles JC, McLaughlin DJ (1992) Basidial development, life history, and the anamorph of Krigeria eriophori. Mycologia 84:668–678CrossRefGoogle Scholar
  11. Fell W, Statzell AC, Hunter IL, Phaff L (1969) Leucosporidium gen. n., the heterobasidiomycetous stage of several yeasts of the genus Candida. Antonie van Laeuwenhoek 35:433–462CrossRefGoogle Scholar
  12. Fell J, Scorzetti G, Connell L, Craig S (2006) Biodiversity of micro-eukaryotes in Antarctic Dry Valley soils with <5% soil moisture. Soil Biol Biochem 38:3107–3119CrossRefGoogle Scholar
  13. Gomes J, Steiner W (2004) The biocatalytic potential of extremophiles and extremozymes. Food Technol Biotechnol 42:223–235Google Scholar
  14. Hanschke R, Schauer F (1996) Improved ultrastructural preservation of yeast cells for scanning electron microscopy. J Microscopy 184:81–87CrossRefGoogle Scholar
  15. Kirk PM, Cannon PF, David JC, Stalper JA (2001) Dictionary of the fungi. 9th edn. Wallingford, p 655Google Scholar
  16. Krallish I, Gonta S, Savenkova L, Bergauer P, Margesin R (2006) Phenol degradation by immobilized cold-adapted yeast strains of Cryptococcus terreus and Rhodotorula creatinivora. Extremophiles 10:441–449PubMedCrossRefGoogle Scholar
  17. Kreger-van Rij NJW, Veenhuis M (1971) A comparative study of the cell wall structure of basidiomycetous and related yeasts. J Gen Microbiol 68:87–95Google Scholar
  18. Lee JK, Park KS, Park S, Park H, Song YH, Kang SH, Kim HJ (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60:222–228PubMedCrossRefGoogle Scholar
  19. Margesin R, Neuner G, Storey KB (2007) Cold-loving microbes, plants, and animals-fundamental and applied aspects. Naturwissenschaften 94:77–99PubMedCrossRefGoogle Scholar
  20. Marvanova L, Suberkropp K (1990) Camptobasidium hydrophilum and its anamorph, Crucella subtilis: a new heterobasidiomycete from streams. Mycologia 82:208–217CrossRefGoogle Scholar
  21. Müller WH, Montijn RC, Humbel BM, van Aelst AC, Boon EJ, van der Krift TP, Boekhout T (1998) Structural differences between two types of basidiomycete septal pore caps. Microbiology 144:1721–1730PubMedCrossRefGoogle Scholar
  22. Nakagawa T, Yamada K, Miyaji T, Tomizuka N (2002) Cold-active pectinolytic activity of psychrophilic-basidiomycetous yeast Cystofilobasidium capitatum strain PPY-1. J Biosci Bioeng 94:175–177PubMedCrossRefGoogle Scholar
  23. Oerlemans J, Anderson B, Hubbard A, Huybrechts Ph, Knap WH, Johannesson T, Schmeits M, Stroeven AP, van de Wal RSW, Wallinga J, Zuo Z (1998) Modelling the response of glaciers to climate warming. Clim Dyn 14:267–274CrossRefGoogle Scholar
  24. Ohgiya S, Hoshino T, Okuyama H, Tanaka S, Ishizaki K (1999) In: Margesin R, Schinner F (eds) Biotechnological application of cold-adapted microorganisms. Springer, Berlin, pp 17–34Google Scholar
  25. Okuyama H, Morita N, Yumoto I (1999) In: Margesin R, Schinner F (eds) Biotechnological application of cold-adapted microorganisms Springer, Germany, pp 101–115Google Scholar
  26. Pazgier M, Turkiewicz M, Kalinowska H, Bielecki S (2003) The unique cold-adapted extracellular subtilase from psychrophilic yeast Leucosporidium antarcticum. J Mol Catal B 21:39–42CrossRefGoogle Scholar
  27. Raspor P, Zupan J (2006) Yeasts in extreme environment. In: Peter G, Rosa C (eds) The yeast handbook biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 371–417CrossRefGoogle Scholar
  28. Sampaio JP (2011) Leucosporidium Fell, Statzell, Hunter & Phaff (1969). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 1485–1494CrossRefGoogle Scholar
  29. 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 2:53–68CrossRefGoogle Scholar
  30. Sampaio JP, Golubev WI, Fell JW, Gadanho M, Golubev NW (2004) Curvibasidium cygneicollum gen. nov., sp. nov. and Curvibasidium pallidicorallinum sp. nov., novel taxa in the Microbotryomycetidae (Urediniomycetes), and their relationship with Rhodotorula fujisanensis and Rhodotorula nothofagi. Int J Syst Evol Microbiol 54:1401–1407PubMedCrossRefGoogle Scholar
  31. 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 region. FEMS Yeast Res 2:495–517PubMedGoogle Scholar
  32. Shivaji S, Prasad GS (2009) Antarctic yeasts: biodiversity and potential applications. In: Satyanarayana T, Kunze G (eds) Yeast biotechnology: diversity and applications. Springer Science, Berlin, pp 3–18CrossRefGoogle Scholar
  33. Statzell-Tallman A, Fell JW (1998) Leucosporidium Fell, Statzell, Hunter & Phaff. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 670–675Google Scholar
  34. Swann EC, Frieders EM, McLaughlin DJ (1999) Microbotryum, Kriegeria and the changing paradigm in basidiomycete classification. Mycologia 91:51–66CrossRefGoogle Scholar
  35. Swann EC, Frieders EM, McLaughlin DJ (2001) Urediniomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) Systematics and evolution. The mycota VII Part B. Springer, Berlin, pp 37–56Google Scholar
  36. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  37. Thomas Hall SR, Turchetti B, Buzzini P, Branda E, Boekhout T, Theelen B, Watson K (2010) Cold-adapted yeasts from Antarctica and Italian Alps-description of three novel species: Mrakia robertii sp. nov., Mrakia blollopis sp. nov. and Mrakiella niccombsii sp. nov. Extremophiles 14:47–59PubMedCrossRefGoogle Scholar
  38. Thomas-Hall SR (2004) Physiological and biochemical characterisation of antarctic yeast. Ph.D. thesis. School of Biological, Biomedical and Molecular Sciences, The University of New England, AustraliaGoogle Scholar
  39. Thomas-Hall S, Watson K (2002) Cryptococcus nyarrowii sp. nov., a basidiomycetous yeast from Antarctica. Int J Syst Evol Microbiol 52:1033–1038PubMedCrossRefGoogle Scholar
  40. Turchetti B, Buzzini P, Goretti M, Branda E, Diolaiuti G, D’Agata C, Smiraglia C, Vaughan-Martini A (2008) Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbiol Ecol 63:73–83PubMedCrossRefGoogle Scholar
  41. Turkiewicz M, Pazgier M, Kalinowska H, Bielecki S (2003) A cold-adapted extracellular serine proteinase of the yeast Leucosporidium antarcticum. Extremophiles 7:435–442PubMedCrossRefGoogle Scholar
  42. Vishniac HS (2006) Yeast biodiversity in the Antarctic. In: Peter G, Rosa C (eds) The yeast handbook biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 419–440CrossRefGoogle Scholar
  43. Vishniac HS, Takashima M (2010) Rhodotorula arctica sp. nov., a basidiomycetous yeast from Arctic soil. Int J Syst Evol Microbiol 60:1215–1218PubMedCrossRefGoogle Scholar
  44. Weiss M, Bauer R, Begerow D (2004) Spotlights on heterobasidiomycetes. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers in basidiomycote mycology. IHW, Eching, pp 7–78Google Scholar
  45. Yarrow D (1998) Methods for the isolation and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 77–100CrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Benedetta Turchetti
    • 1
    Email author
  • Skye R. Thomas Hall
    • 2
  • Laurie B. Connell
    • 3
  • Eva Branda
    • 1
  • Pietro Buzzini
    • 1
  • Bart Theelen
    • 4
  • Wally H. Müller
    • 5
  • Teun Boekhout
    • 4
  1. 1.Department of Applied Biology and Industrial Yeasts Collection DBVPGUniversity of PerugiaPerugiaItaly
  2. 2.School of Biological SciencesUniversity of New EnglandArmidaleAustralia
  3. 3.School of Marine SciencesUniversity of MaineOronoUSA
  4. 4.Yeast and Basidiomycete ResearchCBS-KNAW Fungal Diversity CentreUtrechtThe Netherlands
  5. 5.Department of Cell BiologyUtrecht UniversityUtrechtThe Netherlands

Personalised recommendations