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Genetic Variation Among Penicillium crustosum Isolates from Arctic and other Ecological Niches

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Abstract

Penicillium crustosum is an important and panglobal contaminant of lipid- and protein-rich foods and feeds. Although it is infrequent in extremely cold environments, we isolated a high number of P. crustosum strains from Arctic coastal, but particularly, subglacial environments in Svalbard, Norway. P. crustosum is extremely consistent in its phenotypic properties, including morphology, physiology, and secondary metabolite production. However, some Arctic isolates differed from other Arctic and non-Arctic strains in their weak growth on creatine and in the production of the secondary metabolite andrastin A. In this study, we characterized genetic variability of P. crustosum strains originating from different Arctic and non-Arctic environments using amplified fragment length polymorphism (AFLP) and, in addition, M13 minisatellite fingerprinting and partial β-tubulin gene sequencing. Most of the Arctic strains (85%) showed a relatively low variability and polymorphism level. They produced nine different AFLP genotypes grouped into two clusters in accordance with glacier origin and creatine utilization. The rest of the Arctic isolates and isolates from various non-Arctic environments displayed a much greater degree of genetic variability. It seems that in stressful glacial environment low microbial genetic variation is represented by only a few adapted genotypes that were not recovered from nonpolar environments.

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References

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

    Google Scholar 

  2. Bruford, MW, Wayne, RK (1993) Microsatellites and their application to population genetic studies. Curr Opin Genet Dev 3: 939–943

    Article  PubMed  CAS  Google Scholar 

  3. Castella, G, Larsen, TO, Cabanes, J, Schmidt, H, Alboresi, A, Niessen, L, Färber, P, Geisen, R (2002) Molecular characterization of ochratoxin A producing strains of the genus Penicillium. Syst Appl Microbiol 25: 74–83

    Article  PubMed  CAS  Google Scholar 

  4. De Barros Lopes, M, Rainieri, S, Henschke, PA, Langridge, P (1999) AFLP fingerprinting for analysis of yeast genetic variation. Int J Syst Bacteriol 49: 915–924

    Article  PubMed  Google Scholar 

  5. Denning, DW, Clemons, KV, Hanson, LH, Stevens, DA (1990) Restriction endonuclease analysis of total cellular DNA of Aspergillus fumigatus isolates of geographically and epidemiologically diverse origin. J Infect Dis 162: 1151–1158

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  8. 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 

  9. Frisvad, JC (1985) Creatine sucrose agar, a differential medium for mycotoxin producing terverticillate Penicillium species. Lett Appl Microbiol 1: 109–113

    Google Scholar 

  10. Frisvad, JC (1993) Modifications on media based on creatine for use in Penicillium and Aspergillus taxonomy. Lett Appl Microbiol 16: 154–157

    CAS  Google Scholar 

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

  12. Frisvad, JC, Lund, F, Elmholt, S (2005) Ochratoxin A producing Penicillium verrucosum isolates from cereals reveal large AFLP fingerprinting variability. J Appl Microbiol 98: 684–692

    Article  PubMed  CAS  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. 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 

  15. Frisvad, JC, Thrane, U (1993) Liquid column chromatography of mycotoxins. J Chromatogr Libr 54: 253–372

    CAS  Google Scholar 

  16. 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 

  17. Glass, NL, Donaldson, GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61: 1323–1330

    PubMed  CAS  Google Scholar 

  18. 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 

  19. 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, pp 127–139

    Google Scholar 

  20. Kis-Papo, T, Oren, A, Nevo, E (2003) Genetic diversity of filamentous fungi under hypersaline stress in the Dead Sea. In: Nevo, E, Oren, A, Wasser, SP (Eds.) Fungal Life in the Dead Sea, Gantner Verlag, Ruggell, pp 314–332

    Google Scholar 

  21. Kumar, S, Tamura, K, Nei, M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinformatics 5: 150–163

    Article  PubMed  CAS  Google Scholar 

  22. Kure, CF, Abeln, ECA, Holst-Jensen, A, Skaar, I (2002) Differentiation of Penicillium commune and Penicillium palitans isolates from cheese and indoor environments of cheese factories using M13 fingerprinting. Food Microbiol 19: 151–157

    Article  CAS  Google Scholar 

  23. Kure, CF, Skaar, I, Holst-Jensen, A, Abeln, ECA (2003) The use of AFLP to relate cheese-contaminating Penicillium strains to specific points in the production plants. Int J Food Microbiol 83: 195–204

    Article  PubMed  CAS  Google Scholar 

  24. Leissner, CEW, Niessen, ML, Vogel, RF (1997) Use of the AFLP technique for the identification and discrimination of Fusarium graminearum. Cer Res Com 25: 555–556

    Google Scholar 

  25. Lund, F, Nielsen, AB, Skouboe, P (2003) Distribution of Penicillium commune isolates in cheese dairies mapped using secondary metabolite profiles, morphotypes, RAPD and AFLP fingerprinting. Food Microbiol 20: 725–734

    Article  CAS  Google Scholar 

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

    Google Scholar 

  27. 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 

  28. Majer, D, Mithen, R, Lewis, BG, Vos, P, Oliver, RP (1996) The use of AFLP fingerprinting for the detection of genetic variation in fungi. Mycol Res 100: 1107–1111

    Article  CAS  Google Scholar 

  29. Männistö MK, Häggblom MM (2006) Characterization of psychrotolerant heterotrophic bacteria from Finnish Lapland. Syst Appl Microbiol 29: 229–243

    Article  PubMed  CAS  Google Scholar 

  30. 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 

  31. Meyer, W, Mitchell, TG, Freedman, EZ, Vilgalys, R (1993) Hybridization probes for conventional DNA fingerprinting used as single primers in the polymerase chain reaction to distinguish strains of Cryptococcus neoformans. J Clin Microbiol 31: 2274–2280

    PubMed  CAS  Google Scholar 

  32. Montiel, D, Dickinson, MJ, Lee, HA, Dyer, PS, Jeenes, DJ, Roberts, IN, James, S, Fuller, LJ, Matsuchima, K, Archer, DB (2003) Genetic differentiation of the Aspergillus section Flavi complex using AFLP fingerprints. Mycol Res 107: 1427–1434

    Article  PubMed  CAS  Google Scholar 

  33. Pavlíček, A, Hrda, S, Flegr, J (1999) FreeTree—freeware program for construction of phylogenetic trees on the basis of distance data and for bootstrap/jackknife analysis of the trees robustness. Application in the RAPD analysis of genus Frenkelia. Folia Biol (Praha) 45: 97–99

    Google Scholar 

  34. Perrone, G, Mulè, G, Susca, A, Battilani, P, Pietri, A, Logrieco, A (2006) Ochratoxin A production and amplified fragment length polymorphism analysis of Aspergillus carbonarius, Aspergillus tubingensis, and Aspergillus niger strains isolated from grapes in Italy. Appl Environ Microbiol 72: 680–685

    Article  PubMed  CAS  Google Scholar 

  35. Pitt, JI (1979) Penicillium crustosum and P. simplicissimum, the correct names for two common species producing tremorgenic mycotoxins. Mycologia 71: 1166–1177

    Article  Google Scholar 

  36. Pitt, JI, Hocking, AD (1999) Fungi and Food Spoilage. Aspen Publishers, Inc., Gaithersburg

    Google Scholar 

  37. Radišek, S, Jakše, J, Simončič, A, Javornik, B (2003) Characterization of Verticillium alboatrum field isolates using pathogenicity data and AFLP analysis. Plant Dis 87: 633–638

    Article  Google Scholar 

  38. Raper, CA, Raper, JR, Miller, RE (1972) Genetic analysis of the life cycle of Agaricus bisporus. Mycologia 64: 1088–1117

    Article  Google Scholar 

  39. Rosendahl, S, Taylor, JW (1997) Development of multiple genetic markers for studies of genetic variation in arbuscular mycorrhizal fungi using AFLP™. Mol Ecol 6: 821–829

    Article  CAS  Google Scholar 

  40. Sampaio, JP, Gadanho, M, Santos, S, Duarte, FL, Pais, C, Fonseca, A, Fell, JW (2001) Polyphasic taxonomy of the basidiomycetous yeast genus Rhodosporidium: Rhodosporidium kratochvilovae and related anamorphic species. Int J Syst Evol Microbiol 51: 1–11

    Google Scholar 

  41. Samson, RA, Hoekstra, ES, Frisvad, JC, Filtenborg, O (2002) Introduction to Food- and Airborne Fungi. Centraalbureau voor Schimmelcultures, Utrecht

    Google Scholar 

  42. 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, Centraalbureau voor Schimmelcultures, Utrecht, pp 283–297

    Google Scholar 

  43. Samson, RA, Seifert, KA, Kuijpers, AFA, Houbraken, JAMP, Frisvad, JC (2004) Phylogenetic analysis of Penicillium subgenus Penicillium using partial β-tubulin sequences. Stud Mycol 49: 175–200

    Google Scholar 

  44. Savelkoul, PHM, Aarts, HJM, de Haas, J, Dijkshoorn, L, Duim, B, Otsen, M, Rademaker, JLW, Schouls, L, Lenstra, JA (1999) Amplified-fragment length polymorphism analysis: the state of an art. J Clin Microbiol 37: 3083–3091

    PubMed  CAS  Google Scholar 

  45. Schmidt, H, Niessen, L, Vogel, RF (2004) AFLP analysis of Fusarium species in the section Sporotrichiella—evidence for Fusarium langsethiae as a new species. Int J Food Microbiol 95: 297–304

    Article  PubMed  CAS  Google Scholar 

  46. 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 

  47. 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 

  48. Sonjak, S, Frisvad, JC, Gunde-Cimerman, N (2006) Penicillium mycobiota in Arctic subglacial ice. Microb Ecol 52: 207–216

    Article  PubMed  Google Scholar 

  49. Tuthill, DE (2004) Genetic variation and recombination in Penicillium miczynskii and Eupenicillium species. Mycol Prog 3: 3–12

    Article  Google Scholar 

  50. Van der Lee, T, de Witte, I, Drenth, A, Alfonso, C, Govers, F (1997) AFLP linkage map of the Oomycete Phytophthora infestans. Fungal Genet Biol 21: 278–291

    Article  PubMed  CAS  Google Scholar 

  51. Vos, P, Hogers, R, Bleeker, M, Reijans, M, van der Lee, T, Hornes, M, Frijters, A, Pot, J, Peleman, J, Kuiper, M, Zabeau, M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23: 4407–4414

    Article  PubMed  CAS  Google Scholar 

  52. Williams, JGK, Kubelik, AR, Livak, KJ, Rafalski, JA, Tingey, SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18: 6531–6535

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Sebastjan Radišek for introductory work with the AFLP technique. The sampling was possible due to Large Scale Facility (LSF) Funds.

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Correspondence to Nina Gunde-Cimerman.

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Sonjak, S., Frisvad, J.C. & Gunde-Cimerman, N. Genetic Variation Among Penicillium crustosum Isolates from Arctic and other Ecological Niches. Microb Ecol 54, 298–305 (2007). https://doi.org/10.1007/s00248-006-9202-1

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