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Phenol degradation and heavy metal tolerance of Antarctic yeasts

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Abstract

In cold environments, biodegradation of organic pollutants and heavy metal bio-conversion requires the activity of cold-adapted or cold-tolerant microorganisms. In this work, the ability to utilize phenol, methanol and n-hexadecane as C source, the tolerance to different heavy metals and growth from 5 to 30 °C were evaluated in cold-adapted yeasts isolated from Antarctica. Fifty-nine percent of the yeasts were classified as psychrotolerant as they could grow in all the range of temperature tested, while the other 41% were classified as psychrophilic as they only grew below 25 °C. In the assimilation tests, 32, 78, and 13% of the yeasts could utilize phenol, n-hexadecane, and methanol as C source, respectively, but only 6% could assimilate the three C sources evaluated. In relation to heavy metals ions, 55, 68, and 80% were tolerant to 1 mM of Cr(VI), Cd(II), and Cu(II), respectively. Approximately a half of the isolates tolerated all of them. Most of the selected yeasts belong to genera previously reported as common for Antarctic soils, but several other genera were also isolated, which contribute to the knowledge of this cold environment mycodiversity. The tolerance to heavy metals of the phenol-degrading cold-adapted yeasts illustrated that the strains could be valuable as inoculant for cold wastewater treatment in extremely cold environments.

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References

  • Abe F, Minegishi H (2008) Global screening of genes essential for growth in high-pressure and cold environments: searching for basic adaptive strategies using a yeast deletion library. Genetics 178:851–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aislabie J, Fraser R, Duncan S, Farrell RL (2001) Effects of oil spills on microbial heterotrophs in Antarctic soils. Polar Biol 24(5):308–313

    Article  Google Scholar 

  • Alcaíno J, Cifuentes V, Baeza M (2015) Physiological adaptations of yeasts living in cold environments and their potential applications. World J Microbiol Biotechnol 31(10):1467–1473

    Article  PubMed  Google Scholar 

  • Alexander M (1999) Biodegradation and bioremediation. Gulf Professional Publishing, Houston

    Google Scholar 

  • Alexieva Z, Ivanova D, Godjevargova T, Atanasov B (2002) Degradation of some phenol derivates by Trichosporon cutaneum R57. Proc Biochem 37:1215–1219

    Article  Google Scholar 

  • ATCM, Antarctic Treaty Consultative Meeting (1991) http://www.ats.aq/e/ep.htm

  • Bargagli R (2008) Environmental contamination in Antarctic ecosystems. Sci Total Environ 400:212–226

    Article  CAS  PubMed  Google Scholar 

  • Bastos AER, Tornisielo VL, Nozawa SR, Trevors JT, Rossi A (2000) Phenol metabolism by two microorganisms isolated from Amazonian forest soil samples. J Ind Microbiol Biotechnol 24(6):403–409

    Article  CAS  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(2):217–241

    Article  CAS  PubMed  Google Scholar 

  • Carrasco M, Rozas JM, 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 Microbiol 12:251

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen K, Lin Y, Chen W, Liu Y (2002) Degradation of phenol by PAA immobilized Candida tropicalis. Enzyme Microb Tech 31:490–497

    Article  CAS  Google Scholar 

  • Connel L, Redman R, Craig S, Scorzetti G, Iszard M, Rodriguez R (2008) Diversity of soil yeasts isolated from south Victoria Land, Antarctica. Microb Ecol 56:448–459

    Article  Google Scholar 

  • Corsolini S (2009) Industrial contaminants in Antarctic biota. J Chromatogr A 1216:598–612

    Article  CAS  PubMed  Google Scholar 

  • Curtosi A, Pelletier E, Vodopivez CL, Mac Cormack WP (2007) Polycyclic aromatic hydrocarbons in soil and surface marine sediment near Jubany Station (Antarctica). Role of permafrost as a low-permeability barrier. Sci Total Environ 383(1–3):193–204

    Article  CAS  PubMed  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 

  • De Souza MJ, Nair S, LokaBharathi PA, Chandramohan D (2006) Metal and antibiotic-resistance in psychrotrophic bacteria from Antarctic marine waters. Ecotoxicology 15:379–384

    Article  PubMed  Google Scholar 

  • Fernández PM, Cabral ME, Delgado OD, Fariña JI, Figueroa LIC (2013) Textile dye polluted waters as an unusual source for selecting chromate-reducing yeasts through Cr(VI)-enriched microcosms. Int Biodeterior Biodegradation 79:28–35

    Article  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 

  • Gibson DT, Koch JR, Kallio RE (1968) Oxidative degradation of aromatic hydrocarbons by microorganisms I. Enzymic formation of catechol from benzene. BioChemistry 7(7):2653–2662

    Article  CAS  PubMed  Google Scholar 

  • Gramss G, Voigt KD, Kirsche B (1999) Degradation of polycyclic aromatic hydrocarbons with three to seven aromatic rings by higher fungi in sterile and unsterile soils. Biodegradation 10(1):51–62

    Article  CAS  PubMed  Google Scholar 

  • Guffogg SP, Thomas-Hall S, Holloway P, Watson K (2004) A novel psychrotolerant member of the hymenomycetous yeasts from Antarctica: Cryptococcus watticus sp. nov. Int J Syst Evol Microbiol 54(1):275–277

    Article  CAS  PubMed  Google Scholar 

  • Hagler AN, Ahearn DG (1981) Rapid diazonium blue B test to detect basidiomycetous yeasts. Int J Syst Evol Microbiol 31(2):204–208

    Google Scholar 

  • Hamid B, Rana RS, Chauhan D, Singh P, Mohiddin FA, Sahay S, Abidi I (2014) Psychrophilic yeasts and their biotechnological applications-a review. Afr J Biotechnol 13(22):2188–2197

    Article  CAS  Google Scholar 

  • Hassan N, Rafiq M, Hayat M, Shah AA, Hasan F (2016) Psychrophilic and psychrotrophic fungi: a comprehensive review. Rev Environ Sci Bio/Tech 15(2):147–172

    Article  Google Scholar 

  • Kurtzman C, Fell JW, Boekhout T (eds) (2011) The yeasts: a taxonomic study. Elsevier, Amsterdam

    Google Scholar 

  • Lana NB, Berton P, Covaci A, Ciocco NF, Barrera Oro E, Atencio A, Altamirano JC (2014) Fingerprint of persistent organic pollutants in tissues of Antarctic notothenioid fish. Sci Total Environ 499:89–98

    Article  CAS  PubMed  Google Scholar 

  • Li JK, Humphrey AE (1989) Kinetic and fluorometric behavior of a phenol fermentation. Biotechnol Lett 11(3):177–182

    Article  CAS  Google Scholar 

  • Libkind D, Brizzio S, Ruffini A, Gadanho M, van Broock M, Sampaio JP (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Antonie Van Leeuwenhoek 84:313–322

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  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 

  • Margesin R, Schinner F (1998) Low-temperature bioremediation of a waste water contaminated with anionic surfactants and fuel oil. Appl Microbiol Biotechnol 49(4):482–486

    Article  CAS  PubMed  Google Scholar 

  • Margesin R, Neuner G, Storey KB (2007) Cold-loving microbes, plants and animals—fundamental and applied aspects. Natur-wisseenschaften 94:77–99

    Article  CAS  Google Scholar 

  • Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39(2):144

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moyer CL, Morita RY (2007) Psychrophiles and psychrotrophs. In: Morita RY (ed) Encyclopaedia of life sciences. Wiley, Chichester, pp 1–6

    Google Scholar 

  • Peck LS, Convey P, Barnes DK (2007) Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biol Rev 81(1):75–109

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rovati JI, Pajot HP, Ruberto L, Mac Cormack W, Figueroa LIC (2013) Polyphenolic substrates and dyes degradation by yeasts from 25 de Mayo/King George Island (Antarctica). Yeast 30(11):459–470

    Article  CAS  PubMed  Google Scholar 

  • Royles J, Amesbury MJ, Convey P, Griffiths H, Hodgson DA, Leng MJ, Charman DJ (2013) Plants and soil microbes respond to recent warming on the Antarctic Peninsula. Curr Biol 17(9):1702–1706

    Article  Google Scholar 

  • Santos VL, Linardi VR (2001) Phenol degradation by yeasts isolated from industrial effluents. J Gen Appl Microbiol 47:213–221

    Article  CAS  PubMed  Google Scholar 

  • Satchanska G, Topalova Y, Dimkov R, Groudeva V, Petrov P, Tsvetanov C, Selenska-Pobell S, Golovinsky E (2015) Phenol degradation by environmental bacteria entrapped in cryogels. Biotechnol Biotechnol Equip 29:514–521

    Article  CAS  Google Scholar 

  • Scorzetti G, Petrescu I, Yarrow D, Fell JW (2000) Cryptococcus adeliensis sp. nov., a xylanase producing basidiomycetous yeast from Antarctica. Antonie Van Leeuwenhoek 77(2):153–157

    Article  CAS  PubMed  Google Scholar 

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

    Chapter  Google Scholar 

  • Singh A, Kumar D, Gaur JP (2012) Continuous metal removal from solution and industrial effluents using Spirogyra biomass-packed column reactor. Water Res 46(3):779–788

    Article  CAS  PubMed  Google Scholar 

  • Suciu I, Cosma C, Todică M, Bolboacă SD, Jäntschi L (2008) Analysis of soil heavy metal pollution and pattern in central Transylvania. Int J Mol Sci 9:434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thavamani P, Megharaj M, Naidu R (2012) Bioremediation of high molecular weight polyaromatic hydrocarbons co-contaminated with metals in liquid and soil slurries by metal tolerant PAHs degrading bacterial consortium. Biodegradation 23:823–835

    Article  CAS  PubMed  Google Scholar 

  • Thomas-Hall SR, Turchetti B, Buzzini P, Branda E, Boekhout T, Theelen B, Watson K (2010) Cold-adapted yeasts from Antarctica and the Italian Alps—description of three novel species: Mrakiarobertii sp. nov., Mrakiablollopis sp. nov. and Mrakiellaniccombsii sp. nov. Extremophiles 14:47–59

    Article  CAS  PubMed  Google Scholar 

  • Turchetti B, Buzzini P, Goretti M, Branda E, Diolaiuti G, D’Agata C, Vaughan-Martini A (2008) Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbiol Ecol 63(1):73–83

    Article  CAS  PubMed  Google Scholar 

  • Vishniac HS, Klinger J (1986) Yeasts in the Antarctic deserts. Perspectives in microbial ecology. Proceedings of the 4th ISME, Slovene Society for Microbiology, Ljubljana, Slovenia, 46–51

  • Viswanath B, Rajesh B, Janardhan A, Kumar AP, Narasimha G (2014). Fungal laccases and their applications in bioremediation. Enzyme Res 2014(163242):21. doi:10.1155/2014/163242

    Google Scholar 

  • Wong KK, Quilty B, Hamzah A, Surif S (2015) Phenol biodegradation and metal removal by a mixed bacterial consortium. Bioremediat J 19:104–112

    Article  CAS  Google Scholar 

  • Zalar P, Gunde-Cimerman N (2014) Cold-adapted yeasts in Arctic habitats. In Cold-adapted Yeasts. Springer, Heidelberg, pp. 49–74

    Book  Google Scholar 

  • Zhang T, Zhang YQ, Liu HY, Su J, Zhao LX, Yu LY (2014) Cryptococcus fildesensis sp. nov., a psychrophilic basidiomycetous yeast isolated from Antarctic moss. Int J Syst Evol Microbiol 64(2):675–679

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Instituto Antártico Argentino/Dirección Nacional del Antártico (IAA/DNA), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Agencia Nacional de Promoción Cientifica y Tecnologica (ANPCyT), Universidad de Buenos Aires (UBA), and Universidad Nacional de Tucumán (UNT).

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    Authors and Affiliations

    1. Planta Piloto de Procesos Industriales Microbiológicos (PROIMI-CONICET), San Miguel de Tucumán, Argentina

      Pablo Marcelo Fernández, Mariana G. Blaser & Lucía Inés Castellanos de Figueroa

    2. Instituto Antártico Argentino (IAA), Buenos Aires, Argentina

      María Martha Martorell, Lucas Adolfo Mauro Ruberto & Walter Patricio Mac Cormack

    3. Universidad de Buenos Aires (UBA), Buenos Aires, Argentina

      Lucas Adolfo Mauro Ruberto & Walter Patricio Mac Cormack

    4. NANOBIOTEC-CONICET, Buenos Aires, Argentina

      Lucas Adolfo Mauro Ruberto & Walter Patricio Mac Cormack

    5. Universidad Nacional de Tucumán (UNT), San Miguel de Tucumán, Argentina

      Lucía Inés Castellanos de Figueroa

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    1. Pablo Marcelo Fernández
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    Correspondence to María Martha Martorell.

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    Communicated by A. Driessen.

    P. M. Fernández and M. M. Martorell contributed equally to the work.

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    Fernández, P.M., Martorell, M.M., Blaser, M.G. et al. Phenol degradation and heavy metal tolerance of Antarctic yeasts. Extremophiles 21, 445–457 (2017). https://doi.org/10.1007/s00792-017-0915-5

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