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Penicillium Mycobiota in Arctic Subglacial Ice

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Abstract

Fungi have been only rarely isolated from glacial ice in extremely cold polar regions and were in these cases considered as random, long-term preserved Aeolian deposits. Fungal presence has so far not been investigated in polar subglacial ice, a recently discovered extreme habitat reported to be inhabited exclusively by heterotrophic bacteria. In this study we report on the very high occurrence (up to 9000 CFU L−1) and diversity of filamentous Penicillium spp. in the sediment-rich subglacial ice of three different polythermal Arctic glaciers (Svalbard, Norway). The dominant species was P. crustosum, representing on the average half of all isolated strains from all three glaciers. The other most frequently isolated species were P. bialowiezense, P. chrysogenum, P. thomii, P. solitum, P. palitans, P. echinulatum, P. polonicum, P. commune, P. discolor, P. expansum, and new Penicillium species (sp. 1). Twelve more Penicillium species were occasionally isolated. The fungi isolated produced consistent profiles of secondary metabolites, not different from the same Penicillium species from other habitats. This is the first report on the presence of large populations of Penicillium spp. in subglacial sediment-rich ice.

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References

  1. Abdel-Hafez, SII, Mohawed, SM, El-Said, AHM (1989) Seasonal fluctuations of soil fungi of Wadi Qena at eastern desert of Egypt. Acta Mycol 25: 113–125

    Google Scholar 

  2. Abyzov, SS (1993) Microorganisms in the Antarctic ice. In: Friemann, EI (Ed.) Antarctic Microbiology. Wiley-Liss, Inc., New York, pp 265–295

    Google Scholar 

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

    Google Scholar 

  4. Broady, PA, Weinstein, RN (1998) Algae, lichens and fungi in La Gorce Mountains, Antarctica. Antarct Sci 10: 376–385

    Article  Google Scholar 

  5. Christensen, M, Frisvad, JC, Tuthill, DE (2000) Penicillium species diversity in soil and some taxonomic and ecological notes. In: Samson, RA, Pitt, JI (Eds.) Integration of Modern Taxonomic Methods for Penicillium and Aspergillus Classification. Harwood Academic Publishers, Amsterdam, pp 309–320

    Google Scholar 

  6. Christner, BC, Mosley-Thompson, E, Thompson, LG, Reeve, J (2003) Bacterial recovery from ancient glacial ice. Environ Microbiol 5: 433–436

    Article  PubMed  CAS  Google Scholar 

  7. 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 

  8. Dmitriev, VV, Gilichinski, 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 

  9. Domsch, KH, Gams, W, Anderson, TH (1980) Compendium of Soil Fungi. Academic Press, London, pp 540–611

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  11. Fahnestock, M (2003) Geophysics: glacial flow goes seismic. Science 302: 578–579

    Article  PubMed  CAS  Google Scholar 

  12. Fisher, PJ, Graf, F, Petrini, LE, Sutton, BC, Wookey, PA (1995) Fungal endophytes of Dryas octopetala from a high arctic polar semidesert and from the Swiss Alps. Mycologia 87: 319–323

    Article  Google Scholar 

  13. 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 

  14. Frisvad, JC (2004) Chemical diversity of psychrotolerant fungi. In: Watanabe, MM, Suzuki, K, Seki, T (Eds.) Innovative Roles of Biological Resources Centers. Japan Society for Culture Collections and Worlds Federation of Culture Collections, Tsukuba, pp 165–167

  15. Frisvad, JC, Filtenborg, O, Lund, F, Samson, RA (2000) The homogeneous species and series in subgenus Penicillium are related to mammal nutrition and excretion. In: Samson, RA, Pitt, JI (Eds.) Integration of Modern Taxonomic Methods for Penicillium and Aspergillus Classification. Harwood Academic Publishers, Amsterdam, pp 265–283

    Google Scholar 

  16. Frisvad, JC, Samson, RA (2004) Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol 49: 1–173

    Google Scholar 

  17. Frisvad, JC, Smedsgaard, J, Larsen, TO, Samson, RA (2004) Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud Mycol 49: 201–241

    Article  Google Scholar 

  18. Frisvad, JC, Thrane, U (1987) Standardized high-performance liquid chromatography of 182 mycotoxins and other fungal metabolites based on alkylphenone retention indices and UV–VIS spectra (diode array detection). J Chromatogr 404: 195–214

    Article  PubMed  CAS  Google Scholar 

  19. Frisvad, JC, Thrane, U (1993) Liquid column chromatography of mycotoxins. In: Betina, V (Ed.) Chromatography of Mycotoxins: Techniques and Applications. Elsevier, Amsterdam, pp 253–372

    Google Scholar 

  20. Frisvad, JC, Thrane, U (2002) Mycotoxin production by common filamentous fungi. In: Samson, RA, Hoekstra, ES, Frisvad, JC, Filtenborg, O (Eds.) Introduction to Food- and Airborne Fungi, 6th edn. Centraalbureau voor Schimmelcultures, Baarn, pp 321–330

    Google Scholar 

  21. Gaidos, E, Lanoil, B, Thorsteinsson, T, Graham, A, Skidmore, M, Han, S-K, 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 

  22. Gerrits van den Ende, AHG, de Hoog, GS (1999) Variability and molecular diagnostics of the neurotropic species Cladophialophora bantiana. Stud Mycol 43: 151–162

    Google Scholar 

  23. Golubev, WI (1998) New species of basidiomycetous yeasts, Rhodotorula creatinovora and R. yakutica, isolated from permafrost soils of Eastern-Siberian Arctic. Mykologiya I Phytopathologiya 32: 8–13

    Google Scholar 

  24. 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 Part B 28: 1273–1278

    Article  Google Scholar 

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

    CAS  Google Scholar 

  26. Hocking, AD, Pitt, JI (1980) Dichloran-glycerol medium for enumeration of xerophilic fungi from low-moisture foods. Appl Environ Microbiol 39: 488–492

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  28. Johnson, DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27: 307–317

    Article  CAS  Google Scholar 

  29. King, AD, Hocking, AD, Pitt, JI (1979) Dichloran-rose bengal medium for enumeration and isolation of molds from foods. Appl Environ Microbiol 37: 959–964

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  31. Skidmore, M, Anderson, SP, Sharp, M, Foght, J, Lanoil, BD (2005) Comparison of microbial community compositions of two subglacial environments reveals a possible role for microbes in chemical weathering processes. Appl Environ Microbiol 71: 6986–6997

    Article  PubMed  CAS  Google Scholar 

  32. Lopez-Archilla, AI, Marin, I, Amils, R (2001) Microbial community and ecology of an acidic aquatic environment: the Tinto River, Spain. Microbial Ecol 41: 20–35

    CAS  Google Scholar 

  33. Lopez-Garcia, P, Rodriguez-Valera, F, Pedros-Alio, C, Moreira, D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603–606

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  36. McRae, CF, Hocking, AD, Seppelt, RD (1999) Penicillium species from terrestrial habitats in the Windmill Islands, East Antarctica, including a new species, Penicillium antarcticum. Polar Biol 21: 97–111

    Article  Google Scholar 

  37. O'Donnell, K, Cigelnik, E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7: 103–116

    Article  PubMed  Google Scholar 

  38. Pennisi, E (2003) Microbiology: neither cold nor snow stops tundra fungi. Science 301: 1307

    Article  PubMed  CAS  Google Scholar 

  39. Petrovič, U, Gunde-Cimerman, N, Plemenitaš, A (2002) Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Mol Microbiol 45: 665–672

    Article  Google Scholar 

  40. Pitt, JI, Hocking, AD (1999) Fungi and Food Spoilage, 2nd edn. Aspen Publishers, Inc., Gaithersburg, pp 234, 511, 512

    Google Scholar 

  41. Pitt, JI, Samson, RA, Frisvad, JC (2000) List of accepted species and their synonyms in the family Trichocomaceae. In: Samson, RA, Pitt, JI (Eds.) Integration of Modern Taxonomic Methods for Penicillium and Aspergillus Classification. Harwood Academic Publishers, Amsterdam, pp 9–47

    Google Scholar 

  42. Rogers, SO, Ma, LJ, Zhao, Y, Theraisnathan, V, Shin, S, Zhang, G, Catranis, CM, Starmer, WT, Castello, JD (2005) Recommendations for elimination of contaminants and authentication of isolates in ancient ice cores. In: Castello, JD, Rogers, SO (Eds.) Life in Ancient Ice. Princeton University Press, Princeton, NJ, pp 5–21

    Google Scholar 

  43. Samson, RA, Hoekstra, ES, Frisvad, JC, Filtenborg, O (2002) Introduction to Food- and Airborne Fungi, 6th edn. Centraalbureau voor Schimmelcultures, Utrecht, pp 174–243

    Google Scholar 

  44. Samson, RA, Hoekstra, ES, Lund, F, Filtenborg, O, Frisvad, JC (2002) Methods for the detection, isolation and characterization of food-borne fungi. In: Samson, RA, Hoekstra, ES, Frisvad, JC, Filtenborg, O (Eds.) Introduction to Food- and Airborne Fungi, 6th edn. Centraalbureau Voor Schimmelcultures, Utrecht, pp 283–297

    Google Scholar 

  45. 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 

  46. Siegert, MJ, Ellis-Evans, JC, Tranter, M, Mayer, C, Petit, JR, Salamatin, A, Priscu, JC (2001) Physical, chemical and biological processes in Lake Vostok and other Antarctic subglacial lakes. Nature 414: 603–609

    Article  PubMed  CAS  Google Scholar 

  47. 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 

  48. Smedsgaard, J (1997) Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. J Chromatogr 760: 264–270

    Article  CAS  Google Scholar 

  49. Soinam, VS, Vorobyova, EA, Suzina, NE, Dimitriev, VV, Faizutdinova, RN, Duda, VI, Vishnivetskaya, TA, Ostroumova, NV, Gilichinsky, DA (2000) Viable ancient permafrost yeast. In: Van Dijken, JP, Scheffers, WA (Eds.) The Rising Power of Yeasts in Science and Industry, ISY 2000, Tenth International Symposium on Yeasts, 27 Aug–1 Sept, Papendal, Arnhem, the Netherlands. University Press, Delft, p 140

    Google Scholar 

  50. Sonjak, S, Frisvad, JC, Gunde-Cimerman, N (2005) Comparison of secondary metabolite production by Penicillium crustosum strains, isolated from Arctic and other various ecological niches. FEMS Microbiol Ecol 53: 51–60

    Article  PubMed  CAS  Google Scholar 

  51. Sterflinger, K (1998) Temperature and NaCl-tolerance of rock inhabiting meristematic fungi. Antonie van Leeuwenhoek 74: 271–281

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  53. Vishniac, HS (1993) The microbiology of Antarctic soils. In: Friedman, EI (Ed.) Antarctic Microbiology. Wiley-Liss, Inc., New York, pp 297–341

    Google Scholar 

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Acknowledgments

The work in Ny-Ålesund was funded by EU Large-Scale Facility Fund. Laboratory experiments were partially supported by a FEMS Fellowship and partly by EU under the Major Research Infrastructure (MRI) Centre for Advanced Food Studies (LMC). We also thank the Danish Technical Research Council for support of the Program for Predictive Biotechnology and Center for Microbial Biotechnology.

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Sonjak, S., Frisvad, J.C. & Gunde-Cimerman, N. Penicillium Mycobiota in Arctic Subglacial Ice. Microb Ecol 52, 207–216 (2006). https://doi.org/10.1007/s00248-006-9086-0

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