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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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
Abyzov, SS (1993) Microorganisms in the Antarctic ice. In: Friemann, EI (Ed.) Antarctic Microbiology. Wiley-Liss, Inc., New York, pp 265–295
Babjeva, I, Reshetova, I (1998) Yeast resources in natural habitats at polar circle latitude. Food Technol Biotechnol 36: 1–5
Broady, PA, Weinstein, RN (1998) Algae, lichens and fungi in La Gorce Mountains, Antarctica. Antarct Sci 10: 376–385
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
Christner, BC, Mosley-Thompson, E, Thompson, LG, Reeve, J (2003) Bacterial recovery from ancient glacial ice. Environ Microbiol 5: 433–436
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
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
Domsch, KH, Gams, W, Anderson, TH (1980) Compendium of Soil Fungi. Academic Press, London, pp 540–611
Ekström, G, Nettles, M, Abers, GA (2003) Glacial earthquakes. Science 302: 622–624
Fahnestock, M (2003) Geophysics: glacial flow goes seismic. Science 302: 578–579
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
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
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
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
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
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
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
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
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
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
Gerrits van den Ende, AHG, de Hoog, GS (1999) Variability and molecular diagnostics of the neurotropic species Cladophialophora bantiana. Stud Mycol 43: 151–162
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
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
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
Hocking, AD, Pitt, JI (1980) Dichloran-glycerol medium for enumeration of xerophilic fungi from low-moisture foods. Appl Environ Microbiol 39: 488–492
Ito, H, Koduh, S (1997) Characteristics of water in Kongsfjorden, Svalbard. Proc NIPR Symp Polar Meteorol Glaciol 11: 221–232
Johnson, DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27: 307–317
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
Knight, PG (1997) The basal ice layers of glaciers and ice sheets. Quat Sci Rev 16: 975–993
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
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
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
Ma, L, Catranis, CM, Starmer, WT, Rogers, SO (1999) Revival and characterization of fungi from ancient polar ice. Mycologist 13: 70–73
Ma, L, Rogers, SO, Catranis, CM, Starmer, WT (2000) Detection and characterization of ancient fungi entrapped in glacial ice. Mycologia 92: 286–295
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
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
Pennisi, E (2003) Microbiology: neither cold nor snow stops tundra fungi. Science 301: 1307
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
Pitt, JI, Hocking, AD (1999) Fungi and Food Spoilage, 2nd edn. Aspen Publishers, Inc., Gaithersburg, pp 234, 511, 512
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
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
Samson, RA, Hoekstra, ES, Frisvad, JC, Filtenborg, O (2002) Introduction to Food- and Airborne Fungi, 6th edn. Centraalbureau voor Schimmelcultures, Utrecht, pp 174–243
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
Schadt, CW, Martin, AP, Lipson, DA, Schmidt, SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301: 1359–1361
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
Skidmore, ML, Foght, JM, Sharp, MJ (2000) Microbial life beneath a high Arctic glacier. Appl Environ Microbiol 66: 3214–3220
Smedsgaard, J (1997) Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. J Chromatogr 760: 264–270
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
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
Sterflinger, K (1998) Temperature and NaCl-tolerance of rock inhabiting meristematic fungi. Antonie van Leeuwenhoek 74: 271–281
Tosil, S, Casado, B, Gerdol, R, Caretta, G (2002) Fungi isolated from Antarctic mosses. Polar Biol 25: 262–268
Vishniac, HS (1993) The microbiology of Antarctic soils. In: Friedman, EI (Ed.) Antarctic Microbiology. Wiley-Liss, Inc., New York, pp 297–341
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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DOI: https://doi.org/10.1007/s00248-006-9086-0