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Yeast Activities Involved in Carbon and Nitrogen Cycles in Antarctica

  • Silvana Vero
  • Gabriela Garmendia
  • Adalgisa Martínez-Silveira
  • Ivana Cavello
  • Michael Wisniewski
Chapter
Part of the Springer Polar Sciences book series (SPPS)

Abstract

Antarctica and sub-Antarctic regions are characterized by extreme conditions for life such as low temperatures and nutrient availability, high solar irradiation, and dryness; however, microorganisms from the three domains of life have been found as common inhabitants of soils and waters from those zones. Despite bacteria being the most numerous microorganisms in those habitats, a great diversity of psychrotrophic and psychrophilic yeasts have been also isolated and described. Yeasts, as chemoheterotrophic microorganisms, are involved in the recycling and mineralization of organic matter, playing an important role in carbon cycle. The range of organic substrates that they can degrade is wide. Their ability to produce extracellular hydrolytic enzymes involved in the breakdown of natural organic polymers has been well documented. Moreover, they can also use other substrates as n-alkanes or polyphenolic compounds as a sole carbon and energy source, so they could play a role in bioremediation in human-impacted areas. Most yeast obtain their energy by aerobic respiration; however, in anaerobic conditions, some of them carry out fermentation or anaerobic respiration. The use of nitrate or nitrite as the final electron acceptor provides nitrous oxide (a greenhouse gas) as an end product. Thus, those yeasts can be considered as denitrifying microorganisms playing an important role in the nitrogen cycle.

Keywords

Psychrotrophic and psychrophilic yeasts Carbon biogeochemical cycling Nitrogen biogeochemical cycling Phosphorus biogeochemical cycling Production of extracellular enzymes 

References

  1. Aislabie, J., McLeod, M., & Fraser, R. (1998). Potential for biodegradation of hydrocarbons in soil from the Ross Dependency, Antarctica. Applied Microbiology and Biotechnology, 49, 210–214.  https://doi.org/10.1007/s002530051160.CrossRefGoogle Scholar
  2. Arenz, B. E., Held, B. W., Jurgens, J. A., Farrell, R. L., & Blanchette, R. A. (2006). Fungal diversity in soils and historic wood from the Ross Sea Region of Antarctica. Soil Biology and Biochemistry, 38, 3057–3064.  https://doi.org/10.1016/j.soilbio.2006.01.016.CrossRefGoogle Scholar
  3. Arrarte, E., Garmendia, G., Rossini, C., Wisniewski, M., & Vero, S. (2017). Volatile organic compounds produced by Antarctic strains of Candida sake play a role in the control of postharvest pathogens of apples. Biological Control, 109, 14–20.CrossRefGoogle Scholar
  4. Ballester-Tomás, L., Prieto, J. A., Gil, J. V., Baeza, M., & Randez-Gil, F. (2017). The Antarctic yeast Candida sake: Understanding cold metabolism impact on wine. International Journal of Food Microbiology, 245, 59–65.  https://doi.org/10.1016/j.ijfoodmicro.2017.01.009.CrossRefPubMedGoogle Scholar
  5. Bernhard, A. (2010). The nitrogen cycle: Processes. Nat Educ Knowl, 2, 1–8.Google Scholar
  6. Bhutada, G., Kavšček, M., Ledesma-Amaro, R., Thomas, S., Rechberger, G. N., Nicaud, J. M., & Natter, K. (2017). Sugar versus fat: Elimination of glycogen storage improves lipid accumulation in Yarrowia lipolytica. FEMS Yeast Research, 17, fox020.  https://doi.org/10.1093/femsyr/fox020.CrossRefPubMedCentralGoogle Scholar
  7. Białkowska, A. M., Szulczewska, K. M., Krysiak, J., Florczak, T., Gromek, E., Kassassir, H., Kur, J., & Turkiewicz, M. (2017). Genetic and biochemical characterization of yeasts isolated from Antarctic soil samples. Polar Biology, 40, 1787–1803.CrossRefGoogle Scholar
  8. Brizzio, S., Turchetti, B., De Garcia, V., Libkind, D., Buzzini, P., & Van Broock, M. (2007). Extracellular enzymatic activities of basidiomycetous yeasts isolated from glacial and subglacial waters of Northwest Patagonia (Argentina). Canadian Journal of Microbiology, 53, 519–525.CrossRefGoogle Scholar
  9. Buzzini, P., & Margesin, R. (2014). Cold-adapted yeasts: A lesson from the cold and a challenge for the XXI century. In Cold-adapted yeasts: Biodiversity, adaptation strategies and biotechnological significance (pp. 3–22). Berlin: Springer.CrossRefGoogle Scholar
  10. Buzzini, P., Branda, E., Goretti, M., & Turchetti, B. (2012). Psychrophilic yeasts from worldwide glacial habitats: Diversity, adaptation strategies and biotechnological potential. FEMS Microbiology Ecology, 82, 217–241.CrossRefGoogle Scholar
  11. Buzzini, P., Turk, M., Perini, L., Turchetti, B., & Gunde-Cimerman, N. (2017). Yeasts in polar and subpolar habitats. In Yeasts in natural ecosystems: Diversity (pp. 331–365). Berlin: Springer.CrossRefGoogle Scholar
  12. Carrasco, M., Rozas, J. M., Barahona, S., Alcaíno, J., Cifuentes, V., & Baeza, M. (2012). Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiology, 12, 251.  https://doi.org/10.1186/1471-2180-12-251.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Carrasco, M., Villarreal, P., Barahona, S., Alcaíno, J., Cifuentes, V., & Baeza, M. (2016). Screening and characterization of amylase and cellulase activities in psychrotolerant yeasts. BMC Microbiology, 16, 21.  https://doi.org/10.1186/s12866-016-0640-8.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chen, J., Vandelle, E., Bellin, D., & Delledonne, M. (2014). Nitric oxide detection and function of nitric oxide during the hypersensitive response in Arabidopsis thaliana: Where there’s a will there’s a way. Nitric Oxide, 43, 81–88.  https://doi.org/10.1016/j.niox.2014.06.008.CrossRefPubMedGoogle Scholar
  15. Connell, L., Redman, R., Craig, S., Scorzetti, G., Iszard, M., & Rodriguez, R. (2008). Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microbial Ecology, 56, 448–459.  https://doi.org/10.1007/s00248-008-9363-1.CrossRefPubMedGoogle Scholar
  16. Connell, L. B., Rodriguez, R. R., Redman, R. S., & Dalluge, J. J. (2014). Cold-adapted yeasts in Antarctic deserts. In Cold-adapted yeasts (pp. 75–98). Berlin: Springer.CrossRefGoogle Scholar
  17. Corsolini, S. (2009). Industrial contaminants in Antarctic biota. Journal of Chromatography. A, 1216, 598–612.CrossRefGoogle Scholar
  18. Crenshaw, C. L., Lauber, C., Sinsabaugh, R. L., & Stavely, L. K. (2008). Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry, 87, 17–27.  https://doi.org/10.1007/s10533-007-9165-4.CrossRefGoogle Scholar
  19. Cui, M., Ma, A., Qi, H., Zhuang, X., & Zhuang, G. (2015). Anaerobic oxidation of methane: An “active” microbial process. Microbiologyopen, 4, 1–11.CrossRefGoogle Scholar
  20. De García, V., Brizzio, S., Libkind, D., Buzzini, P., & Van Broock, M. (2007). Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiology Ecology, 59, 331–341.CrossRefGoogle Scholar
  21. de Jesus H. E., & Peixoto, R. S. (2015) Bioremediation in Antarctic soils. Journal of Petroleum and Environmental Biotechnology, 6.  https://doi.org/10.4172/2157-7463.1000248.
  22. Domínguez De María, P., Carboni-Oerlemans, C., Tuin, B., Bargeman, G., Van Der Meer, A., & Van Gemert, R. (2005). Biotechnological applications of Candida antarctica lipase A: State-of-the-art. Journal of Molecular Catalysis B: Enzymatic, 37, 36–46.  https://doi.org/10.1016/j.molcatb.2005.09.001.CrossRefGoogle Scholar
  23. Duarte, A. W. F., Dayo-Owoyemi, I., Nobre, F. S., Pagnocca, F. C., Chaud, L. C. S., Pessoa, A., Felipe, M. G. A., & Sette, L. D. (2013). Taxonomic assessment and enzymes production by yeasts isolated from marine and terrestrial Antarctic samples. Extremophiles, 17, 1023–1035.  https://doi.org/10.1007/s00792-013-0584-y.CrossRefPubMedGoogle Scholar
  24. Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., De Montigny, J., Marck, C., Neuvéglise, C., & Talla, E. (2004). Genome evolution in yeasts. Nature, 430, 35.CrossRefGoogle Scholar
  25. Farese, R. V., Jr., & Walther, T. C. (2009). Lipid droplets finally get a little RESPECT. Cell, 139, 855–860.CrossRefGoogle Scholar
  26. Fernández, P. M., Martorell, M. M., Blaser, M. G., Ruberto, L. A. M., de Figueroa, L. I. C., & Mac Cormack, W. P. (2017). Phenol degradation and heavy metal tolerance of Antarctic yeasts. Extremophiles, 21, 445–457.  https://doi.org/10.1007/s00792-017-0915-5.CrossRefPubMedGoogle Scholar
  27. Gorfer, M., Blumhoff, M., Klaubauf, S., Urban, A., Inselsbacher, E., Bandian, D., Mitter, B., Sessitsch, A., Wanek, W., & Strauss, J. (2011). Community profiling and gene expression of fungal assimilatory nitrate reductases in agricultural soil. The ISME Journal, 5, 1771–1783.  https://doi.org/10.1038/ismej.2011.53.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gorfer, M., Klaubauf, S., Berger, H., & Strauss, J. (2014). The fungal contribution to the nitrogen cycle in agricultural soils. In Metagenomics microbial nitrogen cycle: Theory, methods and applications (pp. 209–225). Norfolk: Caister Academic Press.Google Scholar
  29. Greben, H. A., Joubert, L. M., Tjatji, M. P., Whites, H. E., & Botha, A. (2007). Biological nitrate removal from synthetic wastewater using a fungal consortium in one stage bioreactors. Water SA, 33, 285–290.  https://doi.org/10.4314/wsa.v33i2.49094.CrossRefGoogle Scholar
  30. Guadalupe-Medina, V., Wisselink, H. W., Luttik, M. A., De Hulster, E., Daran, J. M., Pronk, J. T., & Van Maris, A. J. A. (2013). Carbon dioxide fixation by Calvin-Cycle enzymes improves ethanol yield in yeast. Biotechnology for Biofuels, 6, 125.  https://doi.org/10.1186/1754-6834-6-125.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hayatsu, M., Tago, K., & Saito, M. (2008). Various players in the nitrogen cycle: Diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Science & Plant Nutrition, 54, 33–45.CrossRefGoogle Scholar
  32. Herrera, L. M., García-Laviña, C. X., Marizcurrena, J. J., Volonterio, O., de León, R. P., & Castro-Sowinski, S. (2017). Hydrolytic enzyme-producing microbes in the Antarctic oligochaete Grania sp.(Annelida). Polar Biology, 40(4), 947–953.CrossRefGoogle Scholar
  33. IPCC. (2007). Intergovernmental panel on climate change. Summary for policy makers.Google Scholar
  34. Jordan, F. L., Cantera, J. J. L., Fenn, M. E., & Stein, L. Y. (2005). Autotrophic ammonia-oxidizing bacteria contribute minimally to nitrification in a nitrogen-impacted forested ecosystem. Applied and Environmental Microbiology, 71, 197–206.  https://doi.org/10.1128/AEM.71.1.197-206.2005.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kasana, R. C., & Gulati, A. (2011). Cellulases from psychrophilic microorganisms: A review. Journal of Basic Microbiology, 51, 572–579.CrossRefGoogle Scholar
  36. Kavanagh, K. (2005). Fungal fermentation systems and products. In Fungi: Biology and applications. Hoboken: Wiley.CrossRefGoogle Scholar
  37. Kneip, C., Lockhart, P., Voß, C., & Maier, U. G. (2007). Nitrogen fixation in eukaryotes – New models for symbiosis. BMC Evolutionary Biology, 7, 55.CrossRefGoogle Scholar
  38. Kregiel, D. (2008). Physiology and metabolism of Crabtree-negative yeast Debaryomyces occidentalis. Food Chem Biotechnol, 72, 35–44.Google Scholar
  39. Kurtzman, C. P., Fell, J. W., & Boekhout, T. (2011). The yeasts: A taxonomic study. New York: Elsevier.CrossRefGoogle Scholar
  40. Laughlin, R. J., & Stevens, R. J. (2002). Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Science Society of America Journal, 66, 1540.  https://doi.org/10.2136/sssaj2002.1540.CrossRefGoogle Scholar
  41. Lawley, B., Ripley, S., Bridge, P., & Convey, P. (2004). Molecular analysis of geographic patterns of eukaryotic diversity in Antarctic soils molecular analysis of geographic patterns of eukaryotic diversity in Antarctic soils. American Society for Microbiology, 70, 5963–5972.  https://doi.org/10.1128/AEM.70.10.5963.CrossRefGoogle Scholar
  42. Lo Giudice, A., Casella, P., Bruni, V., & Michaud, L. (2013). Response of bacterial isolates from Antarctic shallow sediments towards heavy metals, antibiotics and polychlorinated biphenyls. Ecotoxicology, 22, 240–250.  https://doi.org/10.1007/s10646-012-1020-2.CrossRefPubMedGoogle Scholar
  43. Madigan, M. T., Martinko, J. M., Stahl, D., & Clark, D. P. (2015). Brock biology of microorganisms. New York: Pearson.Google Scholar
  44. Martinez, A., Cavello, I., Garmendia, G., Rufo, C., Cavalitto, S., & Vero, S. (2016). Yeasts from sub-Antarctic region: Biodiversity, enzymatic activities and their potential as oleaginous microorganisms. Extremophiles, 20, 759–769.  https://doi.org/10.1007/s00792-016-0865-3.CrossRefPubMedGoogle Scholar
  45. Matsui, M., Kawamata, A., Kosugi, M., Imura, S., & Kurosawa, N. (2016). Diversity of proteolytic microbes isolated from Antarctic freshwater lakes and characteristics of their cold-active proteases. Polar Science, 13, 82–90.CrossRefGoogle Scholar
  46. Mayer, A. M., & Staples, R. C. (2002). Laccase: New functions for an old enzyme. Phytochemistry, 60, 551–565.CrossRefGoogle Scholar
  47. McNamara, J. T., Morgan, J. L. W., & Zimmer, J. (2015). A molecular description of cellulose biosynthesis. Annual Review of Biochemistry, 84, 895–921.  https://doi.org/10.1146/annurev-biochem-060614-033930.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Melick, D. R., & Seppelt, R. D. (1992). Loss of soluble carbohydrates and changes in freezing point of Antarctic bryophytes after leaching and repeated freeze-thaw cycles. Antarctic Science, 4, 399–404.  https://doi.org/10.1017/S0954102092000592.CrossRefGoogle Scholar
  49. Melick, D. R., & Seppelt, R. D. (1994). The effect of hydration on carbohydrate levels, pigment content and freezing point of Umbilicaria decussata at a continental Antarctic locality. Cryptogamic Botany, 4, 212–217.Google Scholar
  50. Melick, D. R., Hovenden, M. J., & Seppelt, R. D. (1994). Phytogeography of bryophyte and lichen vegetation in the Windmill Islands, Wilkes Land, continental Antarctica. Vegetation, 111, 71–87.  https://doi.org/10.1007/BF00045578.CrossRefGoogle Scholar
  51. Merico, A., Sulo, P., Piškur, J., & Compagno, C. (2007). Fermentative lifestyle in yeasts belonging to the Saccharomyces complex. The FEBS Journal, 274, 976–989.  https://doi.org/10.1111/j.1742-4658.2007.05645.x.CrossRefPubMedGoogle Scholar
  52. Moliné, M., Libkind, D., Van Broock, M., & Rosa, C. A. (2011). The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctic. Brazilian Journal of Microbiology, 42, 937–947.CrossRefGoogle Scholar
  53. Mothapo, N., Chen, H., Cubeta, M. A., Grossman, J. M., Fuller, F., & Shi, W. (2015). Phylogenetic, taxonomic and functional diversity of fungal denitrifiers and associated N2O production efficacy. Soil Biology and Biochemistry, 83, 160–175.CrossRefGoogle Scholar
  54. Pereyra, V., Martinez, A., Rufo, C., & Vero, S. (2014). Oleaginous yeasts form Uruguay and Antarctica as renewable raw material for diodiesel production. American Journal of Bioscience, 2, 251.  https://doi.org/10.11648/j.ajbio.20140206.20.CrossRefGoogle Scholar
  55. Pfeiffer, T., & Morley, A. (2014). An evolutionary perspective on the Crabtree effect. Frontiers in Molecular Biosciences, 1, 1–6.  https://doi.org/10.3389/fmolb.2014.00017.CrossRefGoogle Scholar
  56. Phillips, R. L., Song, B., McMillan, A. M. S., Grelet, G., Weir, B. S., Palmada, T., & Tobias, C. (2016). Chemical formation of hybrid di-nitrogen calls fungal codenitrification into question. Scientific Reports, 6, 39077.  https://doi.org/10.1038/srep39077.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ramli, A. N. M., Mahadi, N. M., Rabu, A., Murad, A. M. A., Bakar, F. D. A., & Illias, R. M. (2011). Molecular cloning, expression and biochemical characterisation of a cold-adapted novel recombinant chitinase from Glaciozyma antarctica PI12. Microbial Cell Factories, 10, 94.  https://doi.org/10.1186/1475-2859-10-94.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Rao, S., Chan, Y., Lacap, D. C., Hyde, K. D., Pointing, S. B., & Farrell, R. L. (2012). Low-diversity fungal assemblage in an Antarctic dry valleys soil. Polar Biology, 35, 567–574.  https://doi.org/10.1007/s00300-011-1102-2.CrossRefGoogle Scholar
  59. Rashid, F. A. A., Rahim, R. A., & Ibrahim, D. (2010). Identification of lipase-producing psychrophilic yeast, Leucosporidium sp. Internet Journal of Microbiology, 9.Google Scholar
  60. Ratledge, C. (2004). Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie, 86, 807–815.CrossRefGoogle Scholar
  61. Rovati, J. I., Pajot, H. F., Ruberto, L., Mac Cormack, W., & Figueroa, L. I. C. (2013). Polyphenolic substrates and dyes degradation by yeasts from 25 de Mayo/King George Island (Antarctica). Yeast, 30, 459–470.  https://doi.org/10.1002/yea.2982.CrossRefPubMedGoogle Scholar
  62. Selbmann, L., de Hoog, G. S., Zucconi, L., Isola, D., Ruisi, S., Gerrits van den Ende, A. H. G., Ruibal, C., De Leo, F., Urzì, C., & Onofri, S. (2008). Drought meets acid: Three new genera in a dothidealean clade of extremotolerant fungi. Studies in Mycology, 61, 1–20.  https://doi.org/10.3114/sim.2008.61.01.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Shivaji, S., & Prasad, G. S. (2009). Antarctic yeasts: Biodiversity and potential applications. In Yeast biotechnology: Diversity and applications (pp. 3–18). Dordrecht: Springer.CrossRefGoogle Scholar
  64. Shoun, H., Fushinobu, S., Jiang, L., Kim, S.-W., & Wakagi, T. (2012). Fungal denitrification and nitric oxide reductase cytochrome P450nor. Philosophical Transactions of the Royal Society B Biological Sciences, 367, 1186–1194.  https://doi.org/10.1098/rstb.2011.0335.CrossRefPubMedCentralGoogle Scholar
  65. Shouns, H., & Tanimoto, T. (1991). Denitrification by the fungus Fusarium oxysporum and involvement nitrite reduction * of cytochrome P-450 in the respiratory. Biochemistry, 266, 11078–11082.Google Scholar
  66. Simek, M. (2000). Nitrification in soil – Terminology and methodology (review). Rostl Vyroba, 46, 385–395.Google Scholar
  67. Singh, B., & Satyanarayana, T. (2011). Microbial phytases in phosphorus acquisition and plant growth promotion. Physiology and Molecular Biology of Plants, 17, 93–103.CrossRefGoogle Scholar
  68. Siverio, J. M. (2002). Assimilation of nitrate by yeasts. FEMS Microbiology Reviews, 26, 277–284.CrossRefGoogle Scholar
  69. Slot, J. C., & Hibbett, D. S. (2007). Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: A phylogenetic study. PLoS One, 2, e1097.  https://doi.org/10.1371/journal.pone.0001097.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Slot, J. C., Hallstrom, K. N., Matheny, P. B., & Hibbett, D. S. (2007). Diversification of NRT2 and the origin of its fungal homolog. Molecular Biology and Evolution, 24, 1731–1743.  https://doi.org/10.1093/molbev/msm098.CrossRefPubMedGoogle Scholar
  71. Souza, C. P., Almeida, B. C., Colwell, R. R., & Rivera, I. N. G. (2011). The importance of chitin in the marine environment. Marine Biotechnology, 13, 823–830.CrossRefGoogle Scholar
  72. Spott, O., Russow, R., & Stange, C. F. (2011). Formation of hybrid N2O and hybrid N2due to codenitrification: First review of a barely considered process of microbially mediated N-nitrosation. Soil Biology and Biochemistry, 43, 1995–2011.CrossRefGoogle Scholar
  73. Stein, L. Y. (2011). Heterotrophic nitrification and nitrifier denitrification. In Nitrification (pp. 95–114). Washington, DC: ASM Press.CrossRefGoogle Scholar
  74. Szczesna Antczak, M., Kubiak, A., Antczak, T., & Bielecki, S. (2009). Enzymatic biodiesel synthesis – Key factors affecting efficiency of the process. Renewable Energy, 34, 1185–1194.  https://doi.org/10.1016/j.renene.2008.11.013.CrossRefGoogle Scholar
  75. Takasaki, K., Shoun, H., Yamaguchi, M., Takeo, K., Nakamura, A., Hoshino, T., & Takaya, N. (2004). Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol. ASBMB, 279, 12414–12420.  https://doi.org/10.1074/jbc.M313761200.CrossRefGoogle Scholar
  76. Thomas-Hall, S. R., Turchetti, B., Buzzini, P., Branda, E., Boekhout, T., Theelen, B., & Watson, K. (2009). Cold-adapted yeasts from Antarctica and the Italian Alps-description of three novel species: Mrakia robertii sp. nov., Mrakia blollopis sp. nov. and Mrakiella niccombsii sp. nov. Extremophiles, 14, 47–59.  https://doi.org/10.1007/s00792-009-0286-7.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Tsuruta, S., Takaya, N., Zhang, L., Shoun, H., Kimura, K., Hamamoto, M., & Nakase, T. (1998). Denitrification by yeasts and occurrence of cytochrome P450nor in Trichosporon cutaneum. FEMS Microbiology Letters, 168, 105–110.CrossRefGoogle Scholar
  78. 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 Microbiology Ecology, 63, 73–83.  https://doi.org/10.1111/j.1574-6941.2007.00409.x.CrossRefPubMedGoogle Scholar
  79. Turkiewicz, M., Pazgier, M., Kalinowska, H., & Bielecki, S. (2003). A cold-adapted extracellular serine proteinase of the yeast Leucosporidium antarcticum. Extremophiles, 7, 435–442.  https://doi.org/10.1007/s00792-003-0340-9.CrossRefPubMedGoogle Scholar
  80. Uetake, J., Yoshimura, Y., Nagatsuka, N., & Kanda, H. (2012). Isolation of oligotrophic yeasts from supraglacial environments of different altitude on the Gulkana Glacier (Alaska). FEMS Microbiology Ecology, 82, 279–286.  https://doi.org/10.1111/j.1574-6941.2012.01323.x.CrossRefPubMedGoogle Scholar
  81. Vaz, A. B. M., Rosa, L. H., Vieira, M. L. A., de Garcia, V., Brandão, L. R., Teixeira, L. C. R., Moliné, M., Libkind, D., Van Broock, M., & Rosa, C. A. (2011). The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Brazilian Journal of Microbiology, 42, 937–947.CrossRefGoogle Scholar
  82. Vishniac, H. S. (2006). Yeast biodiversity in the Antarctic. In Biodiversity and ecophysiology (pp. 419–440). London: Springer.  https://doi.org/10.1007/3-540-30985-3_16.CrossRefGoogle Scholar
  83. Walton, D. W. H. (1985). Cellulose decomposition and its relationship to nutrient cycling at South Georgia (pp. 192–199). New York: Antarctica Nutrient Cycles and Food Webs.  https://doi.org/10.1007/978-3-642-82275-9_27.CrossRefGoogle Scholar
  84. Ward, B. B. (2008). Nitrification in marine systems. In Nitrogen in the marine environment (pp. 199–261). Amsterdam: Elsevier.CrossRefGoogle Scholar
  85. Weinstein, R. N., Montiel, P. O., & Johnstone, K. (2000). Influence of growth temperature on lipid and soluble carbohydrate synthesis by fungi isolated from fellfield soil in the maritime Antarctic. Mycologia, 92, 222–229.  https://doi.org/10.2307/3761554.CrossRefGoogle Scholar
  86. Wynn-Williams, D. D. (1990). Ecological aspects of Antarctic microbiology. Advances in Microbial Ecology, 11, 71–146.  https://doi.org/10.1007/978-1-4684-7612-5_3.CrossRefGoogle Scholar
  87. Yergeau, E., Kang, S., He, Z., Zhou, J., & Kowalchuk, G. A. (2007a). Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect126. IsmeJ, 1, 163–179.CrossRefGoogle Scholar
  88. Yergeau, E., Newsham, K. K., Pearce, D. A., & Kowalchuk, G. A. (2007b). Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environmental Microbiology, 9, 2670–2682.  https://doi.org/10.1111/j.1462-2920.2007.01379.x.CrossRefPubMedGoogle Scholar
  89. Zalar, P., & Gunde-Cimerman, N. (2014). Cold-adapted yeasts in arctic habitats. In Cold-adapted yeasts: Biodiversity, adaptation strategies and biotechnological significance (pp. 49–74). Berlin: Springer.CrossRefGoogle Scholar
  90. Zalar, P., Gostinčar, C., de Hoog, G. S., Uršič, V., Sudhadham, M., & Gunde-Cimerman, N. (2008). Redefinition of Aureobasidium pullulans and its varieties. Studies in Mycology, 61, 21–38.  https://doi.org/10.3114/sim.2008.61.02.CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zhang, J., Müller, C., Zhu, T., Cheng, Y., & Cai, Z. (2011). Heterotrophic nitrification is the predominant NO3- production mechanism in coniferous but not broad-leaf acid forest soil in subtropical China. Biology and Fertility of Soils, 47, 533–542.  https://doi.org/10.1007/s00374-011-0567-z.CrossRefGoogle Scholar
  92. Zhou, Z., Takaya, N., Nakamura, A., Yamaguchi, M., Takeo, K., & Shoun, H. (2002). Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. The Journal of Biological Chemistry, 277, 1892–1896.  https://doi.org/10.1074/jbc.M109096200.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Silvana Vero
    • 1
  • Gabriela Garmendia
    • 1
  • Adalgisa Martínez-Silveira
    • 1
  • Ivana Cavello
    • 2
  • Michael Wisniewski
    • 3
  1. 1.Laboratory of Biotechnology, Microbiology Area, Department of Bioscience, Faculty of ChemistryUniversidad de la RepúblicaMontevideoUruguay
  2. 2.Research and Development Center for Industrial FermentationsCINDEFI (CONICET-La Plata, UNLP)La PlataArgentina
  3. 3.USDA-ARS Appalachian Fruit Research StationKearneysvilleUSA

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