Polar Biology

, Volume 35, Issue 5, pp 749–757 | Cite as

Searching for eukaryotic life preserved in Antarctic permafrost

  • L. Zucconi
  • L. Selbmann
  • P. Buzzini
  • B. Turchetti
  • M. Guglielmin
  • J. C. Frisvad
  • S. Onofri
Original Paper

Abstract

Fungi and yeasts isolated in pure culture from Antarctic permafrost collected at different depths in the McMurdo Dry Valleys were identified with cultural, physiological and molecular methods. Fungi belonged to the genera Penicillium, Eurotium, Cladosporium, Alternaria, Engyodonthium, Aureobasidium, Cordyceps, Rhizopus and yeasts to the genera Cryptococcus and Sporidiobolus. All the strains can be defined as mesophilic psychrotolerant. The molecular analyses revealed that these fungal genotypes do not deviate from the global gene pool of fungi commonly spreading worldwide at present, but possible ancestral strains have been found on the base of metabolic profiles.

Keywords

Antarctica Fungi Yeasts Metabolic profiles UV 

Notes

Acknowledgments

These studies were carried out within the framework of the Italian National Programme for Research in Antarctica (PNRA). Authors deeply thank Prof. Ann Vaughan-Martini for her precious scientific and technical skill in the course of the study.

References

  1. ACGR (Associate Committee on Geotechnical Research) (1988) Glossary of permafrost and related ground-ice terms. Permafrost Subcommittee, National Research Council of Canada, Ottawa. Technical Memorandum 142, pp 156Google Scholar
  2. Adlam LS, Balks MR, Seybold CA, Campbell DI (2010) Temporal and spatial variation in active layer depth in the McMurdo Sound Region, Antarctica. Antarct Sci 22(1):45–52CrossRefGoogle Scholar
  3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  4. Andrews JH, Harris RF, Speaer RN, Lau GW, Nordheim EV (1994) Morphogenesis and adhesion of Aureobasidium pullulans. Can J Microbiol 40:6–17CrossRefGoogle Scholar
  5. Arenz BE, Blanchette RA (2011) Distribution and abundance of soil fungi in Antarctica at sites on the Peninsula, Ross Sea Region and McMurdo Dry Valleys. Soil Biol Biochem 43:308–315CrossRefGoogle Scholar
  6. Bergauer P, Fonteyne PA, Nolard N, Schinner F, Margesin R (2005) Biodegradation of phenol and phenol-related compounds by psychrophilic and cold-tolerant alpine yeasts. Chemosphere 59:909–918PubMedCrossRefGoogle Scholar
  7. Bockheim JG, Hall KJ (2002) Permafrost, active-layer dynamics and periglacial environments of continental Antarctica. S Afr J Sci 98:82–90Google Scholar
  8. Bockheim JG, Campbell IB, Guglielmin M, López-Martìnez J (2008) Distribution of Permafrost and Ground Ice in the Antarctic Region In: Kanel DL, KM Hinkel (eds), Proc 9th Intern Conf on Permafrost, University of Alaska Fairbanks, 29 June-3 July 2008, Alaska, USA, Inst. of Northern Engineering, vol 1, pp 125–130Google Scholar
  9. Brack A (2007) Astrobiology: from the origin of life on Earth to life in the Universe. In: Horneck G, Rettberg P (eds) Complete Course in Astrobiology. Wiley, WeinheimGoogle Scholar
  10. Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe. FEMS Microbiol Ecol 72:354–369PubMedCrossRefGoogle Scholar
  11. Buzina W, Braun H, Freudenschuss K, Lackner A, Habermann W, Stammberger H (2003) Fungal biodiversity–as found in nasal mucus. Med Mycol 41:149–161PubMedGoogle Scholar
  12. Finegold L (1996) Molecular and biophysical aspects of adaptation of life to temperatures below the freezing point. Adv Space Res 18:87–95CrossRefGoogle Scholar
  13. Fonseca Á, Inácio J (2006) Phylloplane yeasts. In: Rosa CA, Gábor P (eds) Biodiversity and ecophysiology of yeasts, vol 1. Springer, Berlin, pp 263–301CrossRefGoogle Scholar
  14. Friedmann EI (1994) Permafrost as microbial habitat. In: Gilichinsky D (ed) Viable microorganisms in permafrost. Russian Academy of Sciences, Pushchino, pp 21–26Google Scholar
  15. Frisvad JC, Samson RA (2004) Polyphasic taxonomy of penicillium subgenus penicillium. A guide to identification of the food and air-borne terverticillate penicillia and their mycotoxins. Stud Mycol 49:1–17Google Scholar
  16. Frisvad JC, Thrane U (1987) Standardized high-performance liquid chromatography of 182 mycotoxins and other fungal metabolites based on alkylphenone indices and UV–VIS spectra (diode-array detection). J Chromatogr 404:195–214PubMedCrossRefGoogle Scholar
  17. Frisvad JC, Larsen TO, Dalsgaard PW, Seifert KA, Louis-Seize G, Lyhne EK, Jarvis BB, Fettinger JC, Overy DP (2006) Four psychrotolerant species with high chemical diversity consistently producing cycloaspeptide A, P. jamesonlandense sp. nov., P. ribium sp. nov., P. soppii and P. lanosum. Intern J Syst Evol Microbiol 56:1427–1437CrossRefGoogle Scholar
  18. Gadanho M, Almeida JMF, Sampaio JP (2003) Assessment of yeast diversity in a marine environment in the south of Portugal by microsatellite-primed PCR. Antonie van Leeuwehnoek 84:217–227CrossRefGoogle Scholar
  19. Gilichinsky DA (2002) Permafrost model of extraterrestrial habitat. In: Horneck G, Baumstarck-Khan C (eds) Astrobiology: the quest for the conditions of life. Springer, Berlin, pp 125–142Google Scholar
  20. Gilichinsky DA, Rivkina E, Bakermans C, Shcherbakova V, Petrovskaya L, Ozerskaya S, Ivanushkina N, Kochkina G, Laurinavichuis K, Pecheritsina S, Fattakhova R, Tiedje JM (2005) Biodiversity of cryopegs in permafrost. FEMS Microbiol Ecol 53:117–128PubMedCrossRefGoogle Scholar
  21. Gilichinsky DA, Wilson GS, Friedmann EI, McKay CP, Sletten RS, Rivkina EM, Vishnivetskaya TA, Erokhina LG, Ivanushkina NE, Kochkina GA, Shcherbakova VA, Soina VS, Spirina EV, Vorobyova EA, Fyodorov-Davydov DG, Hallet B, Ozerskaya SM, Sorokovikov VA, Laurinavichyus KS, Shatilovich AV, Chanton JP, Ostroumov VE, Tiedje JM (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiol 7:275–311CrossRefGoogle Scholar
  22. Golubev WI, Sampaio JP, Golubeva EW (2006) Cryptococcus stepposus, a new filobasidiaceous yeast species found in the Prioksko-terrasny biosphere in Russia. Mycol Res 110:957–961PubMedCrossRefGoogle Scholar
  23. Guglielmin M, Balks MR, Adlam LS, Baio F (2011) Permafrost thermal regime from two 30 m deep boreholes in Southern Victoria Land, Antarctica. Permafr Periglacial Process. doi: 10.1002/ppp.715
  24. 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 32:235–240Google Scholar
  25. Gunde-Cimerman N, Sonjak S, Zalar P, Frisvad JC, Diderichsen B, Pleminatš A (2003) Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity. Phys Chem Earth 28:1273–1278CrossRefGoogle Scholar
  26. Hirst JM (1953) Changes in atmospheric spore content: diurnal periodicity and the effects of water. Trans Br Mycol Soc 36:375–393CrossRefGoogle Scholar
  27. Houbraken J, Frisvad JC, Samson RA (2011) Flemming’s penicillin producing strain is not Penicillium chrysogenum but P. rubens. IMA Fungus 2:87–95CrossRefGoogle Scholar
  28. Kochkina GA, Ivanushkina NE, Karasev SG, EYu Gavrish, Gurina LV, Evetushenko LI, Spirina EV, Vorob’eva EA, Gilichinskii DA, Ozerskaya SM (2001) Survival of micromycetes and Actinobacteria of long-term natural cryopreservation. Microbiol 70:356–364CrossRefGoogle Scholar
  29. Kreslavsky MA, Head JW, Marchant DR (2008) Periods of active permafrost layer formation during the geological history of Mars: implications for circum-polar and mid-latitude surface processes. Planet Space Sci 56:289–302CrossRefGoogle Scholar
  30. Larena I, Salazar O, Gonzalez V, Julian MC, Rubio V (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. J Biotechnol 75:187–194PubMedCrossRefGoogle Scholar
  31. 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. Antonie van Leeuwehnoek 84:313–322CrossRefGoogle Scholar
  32. Lydolph MC, Jacobsen J, Arctander P, Gilbert MTP, Gilichinsky DA, Hansen AJ, Willersslev E, Lange L (2005) Beringian Paleoecology Inferred from permafrost-preserved Fungal DNA. Appl Environ Microbiol 71:1012–1017PubMedCrossRefGoogle Scholar
  33. Muller SW (1947) Permafrost or permanently frozen ground and related engineering problems. Edwards JW Inc., Ann ArborGoogle Scholar
  34. Onofri S, Zucconi L, Tosi S (2007) Continental antarctic fungi. IHW-Verlag, Eching bei MünchenGoogle Scholar
  35. Ozerskaya SM, Ivanushkina NE, Kochkina GA, Fattakhova RN, Gilichinskii DA (2004) Mycelian fungi in cryopegs. Int J Astrobiol 3:327–331CrossRefGoogle Scholar
  36. Ozerskaya S, Kochkina G, Ivanushkina N, Gilichinskii DA (2009) Fungi in permafrost. In: Margesin R (ed) Permafrost Soils. Soil Biology 16, Chapter 7. Springer, Berlin, pp 85–95Google Scholar
  37. Panikov NS, Sizova MV (2007) Growth kinetics of microorganisms isolated from Alaskan soil and permafrost in solid media frozen down to −35°C. FEMS Microbiol Ecol 59:500–512PubMedCrossRefGoogle Scholar
  38. Poliakova AV, Chernov II, Panikov NS (2001) Yeast biodiversity in hydromorphic soils with reference to grass-Sphagnum swamp in Western Siberia and the hammocky tundra region (Barrow, Alaska). Mikrobiol 70:714–720Google Scholar
  39. Pryor BM, Gilbertson RL (2000) Molecular phylogenetic relationships amongst Alternaria species and related fungi based upon analysis of nuclear ITS and mt SSU rDNA sequences. Mycol Res 104:1312–1321CrossRefGoogle Scholar
  40. Rivkina E, Friedmann EI, McKay CP, Gilichinsky D (2000) Metabolic activity of permafrost bacteria below the freezing point. Appl Environ Microbiol 66:3230–3233PubMedCrossRefGoogle Scholar
  41. Rivkina E, Laurinavichius K, McGrath J, Tiedje J, Shcherbakova V, Gilichinsky D (2004) Microbial life in permafrost. Adv Space Res 33:1215–1221PubMedCrossRefGoogle Scholar
  42. Rogers SO, Theraisnathan V, Ma LJ, Zhao Y, Zhang G, Shin SG, Castello JD, Starmer WT (2004) Comparison of protocols for decontamination of environmental ice samples for biological and molecular examination. Appl Environ Microbiol 70:2540–2544PubMedCrossRefGoogle Scholar
  43. Samson RA, Hoekstra ES, Frisvad JC (2004) Introduction to Food and Airborne Fungi, 7th edn. Centraalbureau voor Schimmelcultures, UtrechtGoogle Scholar
  44. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Nat Acad Sci 74:5463–5467PubMedCrossRefGoogle Scholar
  45. Scott JA, Untereiner WA, Wong B, Strauss NA, Malloch D (2004) Genotypic variation in Penicillium chrysogenum from indoor environments. Mycologia 96:1095–1105PubMedCrossRefGoogle Scholar
  46. Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic deserts. Stud Mycol 51:1–32Google Scholar
  47. Selbmann L, de Hoog GS, Zucconi L, Isola D, Ruisi S, Gerrits van den Ende AHG, Ruibal C, De Leo F, Urzì C, Onofri S (2008) Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi. Stud Mycol 61:1–20PubMedCrossRefGoogle Scholar
  48. Serdani M, Kang J-C, Andersen B, Crous PW (2002) Characterisation of Alternaria species-groups associated with core rot of apples in South Africa. Mycol Res 106:561–569CrossRefGoogle Scholar
  49. Smedsgaard J (1997) Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. J Chromatogr A 760:264–270PubMedCrossRefGoogle Scholar
  50. Sonjak S, Frisvad JC, Gunde-Cimerman N (2006) Penicillium mycobiota in Arctic subglacial ice. Microbial Ecol 52:207–216CrossRefGoogle Scholar
  51. Steven B, Briggs G, McKay CP, Pollard WH, Greer CW, Whyte LG (2007) Characterization of the microbial diversity in a permafrost sample from the Canadian high Arctic using culture-dependent and culture-independent methods. FEMS Microbiol Ecol 59:513–523PubMedCrossRefGoogle Scholar
  52. Sun F, Shao Z (2007) Biosorption and bioaccumulation of lead by Penicillium sp. Psf-2 isolated from the deep sea sediment of the Pacific Ocean. Extremophiles 11:853–858PubMedCrossRefGoogle Scholar
  53. Tosi S, Onofri S, Brusoni M, Zucconi L, Vishniac H (2005) Response of Antarctic soil fungal assemblages to experimental warming and reduction of UV radiation. Polar Biol 28:470–482CrossRefGoogle Scholar
  54. 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
  55. Urzì C, De Leo F, Lo Passo C, Criseo G (1999) Intra-specific diversity of Aureobasidium pullulans strains isolated from rocks and other habitats assessed by physiological methods and by random amplified polymorphic DNA (RAPD). J Microbiol Methods 36:95–105PubMedCrossRefGoogle Scholar
  56. Valerio E, Gadanho M, Sampaio JP (2008) Reappraisal of the Sporobolomyces roseus species complex and description of Sporidiobolus metaroseus sp. nov. Int J Syst Evol Microbiol 58:736–741PubMedCrossRefGoogle Scholar
  57. Vishniac HS (1993) The microbiology of Antarctic soils. In: Friedmanm I (ed) Antarctic microbiology, Chapter 8. Wiley-Liss, New York, pp 297–341Google Scholar
  58. Vishniac HS (2006) Yeast biodiversity in the Antarctic. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts, Chapter 16. Springer, Berlin, pp 419–440CrossRefGoogle Scholar
  59. Vishnivetskaya TA, Kathariou S, McGrath J, Gilichinsly DA, Tiedje JM (2000) Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments. Extremophiles 4:165–173PubMedCrossRefGoogle Scholar
  60. Vishnivetskaya TA, Petrova MA, Urbance J, Ponder M, Moyer CL, Gilichinsly DA, Tiedje JM (2006) Bacterial community in ancient Siberian permafrost as characterized by culture and culture-independent methods. Astrobiol 6:400–414CrossRefGoogle Scholar
  61. Vorobyova E, Soina V, Gorlenko M, Minkovskaya N, Zalinova N, Mamukelashvili A, Gilichinski D, Rivkina E, Vishnivetskaya T (1997) The deep cold biosphere: facts and hypothesis. FEMS Microbiol Rev 20:277–290CrossRefGoogle Scholar
  62. Wagner D (2008) Microbial communities and processes in Arctic permafrost environments. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Soil Biology vol 13, Chapter 7. Springer, Berlin, pp 133–154Google Scholar
  63. White TJ, Bruns T, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols, a guide to methods and applications. Academic, San Diego, pp 315–322Google Scholar
  64. Willerslev E, Hansen AJ, Poinar HN (2004) Isolation of nucleic acids and cultures from fossil ice and permafrost. Trends Ecol Evol 19:141–147PubMedCrossRefGoogle Scholar
  65. Yarrow D (1998) Methods for the isolation, maintenance and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts. A taxonomic study. Academic, London, pp 77–100CrossRefGoogle Scholar
  66. Zhelifonova VP, Antipova V, Oserskaya SM, Kochkina GA, Kozlovsky AG (2009) Secondary metabolites of Penicillium fungi isolated from permafrost deposits as chemotaxonomic markers. Microbiol (Moscow) 78:393–398Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • L. Zucconi
    • 1
  • L. Selbmann
    • 1
  • P. Buzzini
    • 2
  • B. Turchetti
    • 2
  • M. Guglielmin
    • 3
  • J. C. Frisvad
    • 4
  • S. Onofri
    • 1
  1. 1.Dipartimento di Scienze Ecologiche e BiologicheUniversità degli Studi della Tuscia, Largo dell’Università sncViterboItaly
  2. 2.Dipartimento di Biologia Applicata e Collezione Industriale dei Lieviti DBVPGUniversità di PerugiaPerugiaItaly
  3. 3.Dipartimento di Biologia Funzionale e StrutturaleUniversità dell’InsubriaVareseItaly
  4. 4.Center for Microbial Biotechnology, Department of Systems BiologyTechnical University of DenmarkKgs. LyngbyDenmark

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