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Identification and characterization of yeasts isolated from the South Shetland Islands and the Antarctic Peninsula

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Abstract

Antarctica is considered one of the most extreme environments on Earth because of its low temperatures, dryness, high incidence of solar radiation and low nutrient availability. Nevertheless, microorganisms including yeast have successfully colonized Antarctica; however, little is known about Antarctic yeast. In this study, cultivable yeast from soil samples collected from several islands of the South Shetland archipelago and Antarctic Peninsula were identified and characterized at different levels. Most yeasts were psychrotolerant and belonged to eleven genera, with the majority belonging to the Cryptococcus genus. Most yeasts were able to oxidize dextrin, α-d-glucose, sucrose and d-trehalose and to assimilate turanose, d-xylose, dextrin, d-trehalose, α-d-glucose and salicin. Evaluation of twelve hydrolytic enzymes revealed that yeast isolates displayed four to seven different enzyme activities, with lipase, alkaline phosphatase and invertase activities being observed in the majority of isolates. The isolates identified as Cryptococcus gastricus, Cryptococcus victoriae, Cryptococcus gilvencens, Leucosporidium sp. and Rhodotorula mucilaginosa displayed toxicity against other yeast isolates via the secretion of a protein factor. These results reflect the adaptation of yeast to their environment. The yeasts identified in this study have the potential for use as a biosource for the production of enzymes for industrial applications that require high enzyme activities at low temperatures.

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References

  • Alcaíno J, Cifuentes V, Baeza M (2015) Physiological adaptations of yeasts living in cold environments and their potential applications. World J Microbiol Biotechnol 31:1467–1473

    Article  PubMed  Google Scholar 

  • Amoresano A, Andolfo A, Corsaro MM, Zocchi I, Petrescu I, Gerday C, Marino G (2000) Structural characterization of a xylanase from psychrophilic yeast by mass spectrometry. Glycobiology 10:451–458

    Article  CAS  PubMed  Google Scholar 

  • Arnold RJ, Convey P, Hughes KA, Wynn-Williams DD (2003) Seasonal periodicity of physical factors, inorganic nutrients and microalgae in Antarctic fellfields. Polar Biol 26:396–403

    Google Scholar 

  • Aurilia V, Parracino A, D’Auria S (2008) Microbial carbohydrate esterases in cold adapted environments. Gene 410:234–240

    Article  CAS  PubMed  Google Scholar 

  • Baeza M, Retamales P, Sepulveda D, Lodato P, Jimenez A, Cifuentes V (2009) Isolation, characterization and long term preservation of mutant strains of Xanthophyllomyces dendrorhous. J Basic Microbiol 49:135–141

    Article  CAS  PubMed  Google Scholar 

  • Boyle JS, Lew AM (1995) An inexpensive alternative to glassmilk for DNA purification. Trends Genet 11:8

    Article  CAS  PubMed  Google Scholar 

  • 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). Can J Microbiol 53:519–525

    Article  CAS  PubMed  Google Scholar 

  • Buzzini P, Margesin R (2014) Cold-adapted yeasts. In: Białkowska A, Turkiewicz M (eds) Miscellaneous cold-active yeast enzymes of industrial importance. Springer, New York, pp 377–395

    Google Scholar 

  • Buzzini P, Martini A (2002) Extracellular enzymatic activity profiles in yeast and yeast-like strains isolated from tropical environments. J Appl Microbiol 93:1020–1025

    Article  CAS  PubMed  Google Scholar 

  • Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241

    Article  CAS  PubMed  Google Scholar 

  • Carrasco M, Rozas JM, Barahona S, Alcaino J, Cifuentes V, Baeza M (2012) Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiol 12:251

    Article  PubMed  PubMed Central  Google Scholar 

  • Conti S, Cantelli C, Gerloni M, Fisicaro P, Magliani W, Bertolotti D, Mozzoni P, Sullivan D, Coleman D, Polonelli L (1996) Killer factor interference in mixed opportunistic yeast cultures. Mycopathologia 135:1–8

    Article  CAS  PubMed  Google Scholar 

  • Convey P (1996) The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biol Rev 71:191–225

    Article  Google Scholar 

  • D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389

    Article  PubMed  PubMed Central  Google Scholar 

  • Dahiya N, Tewari R, Hoondal GS (2006) Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol 71:773–782

    Article  CAS  PubMed  Google Scholar 

  • De Mot R, Verachtert H (1987) Purification and characterization of extracellular alpha-amylase and glucoamylase from the yeast Candida antarctica CBS 6678. Eur J Biochem 164:643–654

    Article  PubMed  Google Scholar 

  • Fabiano M, Danovaro R (1999) Meiofauna distribution and mesoscale variability in two sites of the Ross Sea (Antarctica) with contrasting food supply. Polar Biol 22:115–123

    Article  Google Scholar 

  • Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50(Pt 3):1351–1371

    Article  CAS  PubMed  Google Scholar 

  • Fenice M, Selbmann L, Zucconi L, Onofri S (1997) Production of extracellular enzymes by Antarctic fungal strains. Polar Biol 17:275–280

    Article  Google Scholar 

  • Fujita SI, Senda Y, Nakaguchi S, Hashimoto T (2001) Multiplex PCR using internal transcribed spacer 1 and 2 regions for rapid detection and identification of yeast strains. J Clin Microbiol 39:3617–3622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-Martos P, Marín P, Hernández-Molina JM, García-Agudo L, Aoufi S, Mira J (2001) Extracellular enzymatic activity in 11 Cryptococcus species. Mycopathologia 150:1–4

    Article  PubMed  Google Scholar 

  • Gerday C, Aittaleb M, Bentahir M, Chessa JP, Claverie P, Collins T, D’Amico S, Dumont J, Garsoux G, Georlette D (2000) Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol 18:103–107

    Article  CAS  PubMed  Google Scholar 

  • Gomes J, Gomes I, Steiner W (2000) Thermolabile xylanase of the Antarctic yeast Cryptococcus adeliae: production and properties. Extremophiles 4:227–235

    Article  CAS  PubMed  Google Scholar 

  • Gopinath SCB, Anbu P, Hilda A (2005) Extracellular enzymatic activity profiles in fungi isolated from oil-rich environments. Mycoscience 46:119–126

    Article  CAS  Google Scholar 

  • Gounot AM (1986) Psychrophilic and psychrotrophic microorganisms. Experientia 42:1192–1197

    Article  CAS  PubMed  Google Scholar 

  • Hankin L, Anagnostakis SL (1975) The use of solid media for detection of enzyme production by fungi. Mycologia 67:597–607

    Article  Google Scholar 

  • Henderson RJ, Olsen RE, Eilertsen HC (1991) Lipid composition of phytoplankton from the Barents Sea and environmental influences on the distribution pattern of carbon among photosynthetic end products. Polar Res 10:229–238

    Article  Google Scholar 

  • Hodgkins M, Sudbery P, Mead D, Ballance DJ, Goodey A (1993) Expression of the glucose oxidase gene from Aspergillus niger in Hansenula polymorpha and its use as a reporter gene to isolate regulatory mutations. Yeast 9:625–635

    Article  CAS  PubMed  Google Scholar 

  • Holdgate MW (1977) Terrestrial ecosystems in the Antarctic. Philos Trans R Soc B 279:5

    Article  Google Scholar 

  • Horowitz NH, Cameron RE, Hubbard JS (1972) Microbiology of the dry valleys of Antarctica. Adv Sci 176:242–245

    CAS  Google Scholar 

  • Hua MX, Chi Z, Liu GL, Buzdar MA, Chi ZM (2010) Production of a novel and cold-active killer toxin by Mrakia frigida 2E00797 isolated from sea sediment in Antarctica. Extremophiles 14:515–521

    Article  CAS  PubMed  Google Scholar 

  • Kasana RC, Gulati A (2011) Cellulases from psychrophilic microorganisms: a review. J Basic Microbiol 51:572–579

    Article  CAS  PubMed  Google Scholar 

  • Kurtzman CP (2006) Yeast species recognition from gene sequence analyses and other molecular methods. Mycoscience 47:65–71

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. [Epub ahead of print]

  • Kurtzman C, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study, 5th edn. Elsevier, London

    Google Scholar 

  • Kutty SN, Philip R (2008) Marine yeasts-a review. Yeast 25:465–483

    Article  CAS  PubMed  Google Scholar 

  • Magliani W, Conti S, Gerloni M, Bertolotti D, Polonelli L (1997) Yeast killer systems. Clin Microbiol Rev 10:369–400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Magliani W, Conti S, Travassos LR, Polonelli L, Oncologia UD (2008) From yeast killer toxins to antibodies and beyond. FEMS Microbiol Lett 288:1–8

    Article  CAS  PubMed  Google Scholar 

  • Marangon AV, Bertoni TA, Kioshima ES, Falleiros De Padua RA, Venturini S, Svidzinski TI (2003) Dehydrated gelatin drops: a good method for fungi maintenance and preservation. New Microbiol 26:305–309

    CAS  PubMed  Google Scholar 

  • Margesin R, Feller G (2010) Biotechnological applications of psychrophiles. Environ Technol 31:835–844

    Article  CAS  PubMed  Google Scholar 

  • Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361

    Article  PubMed  Google Scholar 

  • McCarthy AJ, Peace E, Broda P (1985) Studies on the extracellular xylanase activity of some thermophilic actinomycetes. Appl Microbiol Biotechnol 21:238–244

    Article  CAS  Google Scholar 

  • Meinhardt F, Klassen R (2009) Yeast killer toxins: fundamentals and applications. In: Anke T, Weber D (eds) The mycota. Springer, Berlin, pp 107–130

    Google Scholar 

  • Morais PB, Rosa CA, Linardi VR, Pataro C, Maia ABRA (1997) Short communication: characterization and succession of yeast populations associated with spontaneous fermentations during the production of Brazilian sugar-cane aguardente. J Microbiol 13:241–243

    Google Scholar 

  • Myrold DD, Zeglin LH, Jansson JK (2014) The potential of metagenomic approaches for understanding soil microbial processes. Soil Sci Soc Am J 78:3

    Article  Google Scholar 

  • Orellana SC (2013) Assessment of fungal diversity in the environment using metagenomics: a decade in review. Fungal Genom Biol 3:1–13

    Article  Google Scholar 

  • Pathan AA, Bhadra B, Begum Z, Shivaji S (2010) Diversity of yeasts from puddles in the vicinity of midre lovenbreen glacier, arctic and bioprospecting for enzymes and fatty acids. Curr Microbiol 60:307–314

    Article  CAS  PubMed  Google Scholar 

  • Polonelli L, Morace G (1986) Reevaluation of the yeast killer phenomenon. J Clin Microbiol 24:866–869

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pulicherla KK, Ghosh M, Kumar PS, Sambasiva Rao KRS (2011) Psychrozymes-the next generation industrial enzymes. J Mar Sci Res Dev 1:2

    Article  Google Scholar 

  • Rankin SA, Christiansen A, Lee W, Banavara DS, Lopez-Hernandez A (2010) Invited review: the application of alkaline phosphatase assays for the validation of milk product pasteurization. J Dairy Sci 93:5538–5551

    Article  CAS  PubMed  Google Scholar 

  • Ray MK, Devi KU, Kumar GS, Shivaji S (1992) Extracellular protease from the Antarctic yeast Candida humicola. Appl Environ Microbiol 58:1918–1923

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rina M, Pozidis C, Mavromatis K, Tzanodaskalaki M, Kokkinidis M, Bouriotis V (2000) Alkaline phosphatase from the Antarctic strain TAB 5. Properties and psychrophilic adaptations. Eur J Biochem 267:1230–1238

    Article  CAS  PubMed  Google Scholar 

  • Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    Article  CAS  Google Scholar 

  • Salek A, Industry F (1990) Transmission of killer activity into laboratory and industrial strains of Saccharomyces cerevisiae by electroinjection. Yeast 70:67–72

    CAS  Google Scholar 

  • Sanchez S, Demain AL (2011) Enzymes and bioconversions of industrial, pharmaceutical, and biotechnological significance. Org Process Res Dev 15:224–240

    Article  CAS  Google Scholar 

  • Shivaji S, Prasad GS (2009) Antarctic yeasts: biodiversity and potential applications. In: Satyanarayana T, Kunze G (eds) Yeast biotechnology: diversity and applications. Springer, Dordrecht, pp 3–18

    Chapter  Google Scholar 

  • Slifkin M (2000) Tween 80 opacity test responses of various Candida species. J Clin Microbiol 38:4626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith VR (2002) Climate change in the sub-Antarctic: an illustration from Marion Island. Clim Change 52:345–357

    Article  CAS  Google Scholar 

  • Strauss ML, Jolly NP, Lambrechts MG, van Rensburg P (2001) Screening for the production of extracellular hydrolytic enzymes by non-Saccharomyces wine yeasts. J Appl Microbiol 91:182–190

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43:777

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 63:73–83

    Article  CAS  PubMed  Google Scholar 

  • Turkiewicz M, Pazgier M, Kalinowska H, Bielecki S (2003) A cold-adapted extracellular serine proteinase of the yeast Leucosporidium antarcticum. Extremophiles 7:435–442

    Article  CAS  PubMed  Google Scholar 

  • Vaz ABM, Rosa LH, Vieira MLA, Garcia VD, Brandao LR, Teixeira LCR, Moliné M, Libkind D, van Broock M, Rosa CA (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica. Braz J Microbiol 42:937–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vishniac HS (1985) Cryptococcus friedmannii, a new species of yeast from the Antarctic. Mycologia 77:149–153

    Article  CAS  PubMed  Google Scholar 

  • Wang QM, Groenewald M, Takashima M, Theelen B, Han PJ, Liu XZ, Boekhout T, Bai FY (2015a) Phylogeny of yeasts and related filamentous fungi within Pucciniomycotina determined from multigene sequence analyses. Stud Mycol 81:27–53

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang QM, Yurkov AM, Göker M, Lumbsch HT, Leavitt SD, Groenewald M, Theelen B, Liu XZ, Boekhout T, Bai FY (2015b) Phylogenetic classification of yeasts and related taxa within Pucciniomycotina. Stud Mycol 81:149–189

    Article  PubMed  Google Scholar 

  • Xu J, Vilgalys R, Mitchell TG (1998) Colony size can be used to determine the MIC of fluconazole for pathogenic yeasts. J Clin Microbiol 36:2383–2385

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by Grant T_07-13 from the Instituto Antártico Chileno.

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Correspondence to Marcelo Baeza.

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Troncoso, E., Barahona, S., Carrasco, M. et al. Identification and characterization of yeasts isolated from the South Shetland Islands and the Antarctic Peninsula. Polar Biol 40, 649–658 (2017). https://doi.org/10.1007/s00300-016-1988-9

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  • DOI: https://doi.org/10.1007/s00300-016-1988-9

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