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Extremophiles

, Volume 21, Issue 3, pp 445–457 | Cite as

Phenol degradation and heavy metal tolerance of Antarctic yeasts

  • Pablo Marcelo Fernández
  • María Martha MartorellEmail author
  • Mariana G. Blaser
  • Lucas Adolfo Mauro Ruberto
  • Lucía Inés Castellanos de Figueroa
  • Walter Patricio Mac Cormack
Original Paper

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.

Keywords

Phenol Heavy metals Bioremediation Tolerance Yeasts Antarctica 

Notes

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).

References

  1. 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 178:851–872CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aislabie J, Fraser R, Duncan S, Farrell RL (2001) Effects of oil spills on microbial heterotrophs in Antarctic soils. Polar Biol 24(5):308–313CrossRefGoogle Scholar
  3. 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):1467–1473CrossRefPubMedGoogle Scholar
  4. Alexander M (1999) Biodegradation and bioremediation. Gulf Professional Publishing, HoustonGoogle Scholar
  5. Alexieva Z, Ivanova D, Godjevargova T, Atanasov B (2002) Degradation of some phenol derivates by Trichosporon cutaneum R57. Proc Biochem 37:1215–1219CrossRefGoogle Scholar
  6. ATCM, Antarctic Treaty Consultative Meeting (1991) http://www.ats.aq/e/ep.htm
  7. Bargagli R (2008) Environmental contamination in Antarctic ecosystems. Sci Total Environ 400:212–226CrossRefPubMedGoogle Scholar
  8. 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):403–409CrossRefGoogle Scholar
  9. 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):217–241CrossRefPubMedGoogle Scholar
  10. 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 12:251CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen K, Lin Y, Chen W, Liu Y (2002) Degradation of phenol by PAA immobilized Candida tropicalis. Enzyme Microb Tech 31:490–497CrossRefGoogle Scholar
  12. 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 56:448–459CrossRefGoogle Scholar
  13. Corsolini S (2009) Industrial contaminants in Antarctic biota. J Chromatogr A 1216:598–612CrossRefPubMedGoogle Scholar
  14. 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):193–204CrossRefPubMedGoogle Scholar
  15. D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389CrossRefPubMedPubMedCentralGoogle Scholar
  16. De Souza MJ, Nair S, LokaBharathi PA, Chandramohan D (2006) Metal and antibiotic-resistance in psychrotrophic bacteria from Antarctic marine waters. Ecotoxicology 15:379–384CrossRefPubMedGoogle Scholar
  17. 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 79:28–35CrossRefGoogle Scholar
  18. 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 18:103–107CrossRefPubMedGoogle Scholar
  19. Gibson DT, Koch JR, Kallio RE (1968) Oxidative degradation of aromatic hydrocarbons by microorganisms I. Enzymic formation of catechol from benzene. BioChemistry 7(7):2653–2662CrossRefPubMedGoogle Scholar
  20. 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):51–62CrossRefPubMedGoogle Scholar
  21. 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):275–277CrossRefPubMedGoogle Scholar
  22. Hagler AN, Ahearn DG (1981) Rapid diazonium blue B test to detect basidiomycetous yeasts. Int J Syst Evol Microbiol 31(2):204–208Google Scholar
  23. 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):2188–2197CrossRefGoogle Scholar
  24. 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):147–172CrossRefGoogle Scholar
  25. Kurtzman C, Fell JW, Boekhout T (eds) (2011) The yeasts: a taxonomic study. Elsevier, AmsterdamGoogle Scholar
  26. 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 499:89–98CrossRefPubMedGoogle Scholar
  27. Li JK, Humphrey AE (1989) Kinetic and fluorometric behavior of a phenol fermentation. Biotechnol Lett 11(3):177–182CrossRefGoogle Scholar
  28. 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 84:313–322CrossRefPubMedGoogle Scholar
  29. 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 22:240–250CrossRefPubMedGoogle Scholar
  30. Margesin R, Feller G (2010) Biotechnological applications of psychrophiles. Environ Technol 31:835–844CrossRefPubMedGoogle Scholar
  31. Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361CrossRefPubMedGoogle Scholar
  32. Margesin R, Schinner F (1998) Low-temperature bioremediation of a waste water contaminated with anionic surfactants and fuel oil. Appl Microbiol Biotechnol 49(4):482–486CrossRefPubMedGoogle Scholar
  33. Margesin R, Neuner G, Storey KB (2007) Cold-loving microbes, plants and animals—fundamental and applied aspects. Natur-wisseenschaften 94:77–99CrossRefGoogle Scholar
  34. Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39(2):144PubMedPubMedCentralGoogle Scholar
  35. Moyer CL, Morita RY (2007) Psychrophiles and psychrotrophs. In: Morita RY (ed) Encyclopaedia of life sciences. Wiley, Chichester, pp 1–6Google Scholar
  36. Peck LS, Convey P, Barnes DK (2007) Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biol Rev 81(1):75–109CrossRefGoogle Scholar
  37. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353CrossRefGoogle Scholar
  38. 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):459–470CrossRefPubMedGoogle Scholar
  39. 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):1702–1706CrossRefGoogle Scholar
  40. Santos VL, Linardi VR (2001) Phenol degradation by yeasts isolated from industrial effluents. J Gen Appl Microbiol 47:213–221CrossRefPubMedGoogle Scholar
  41. 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 29:514–521CrossRefGoogle Scholar
  42. 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):153–157CrossRefPubMedGoogle Scholar
  43. 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 3–18CrossRefGoogle Scholar
  44. 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):779–788CrossRefPubMedGoogle Scholar
  45. 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 9:434CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 23:823–835CrossRefPubMedGoogle Scholar
  47. 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 14:47–59CrossRefPubMedGoogle Scholar
  48. 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):73–83CrossRefPubMedGoogle Scholar
  49. 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, 46–51Google Scholar
  50. 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
  51. Wong KK, Quilty B, Hamzah A, Surif S (2015) Phenol biodegradation and metal removal by a mixed bacterial consortium. Bioremediat J 19:104–112CrossRefGoogle Scholar
  52. Zalar P, Gunde-Cimerman N (2014) Cold-adapted yeasts in Arctic habitats. In Cold-adapted Yeasts. Springer, Heidelberg, pp. 49–74CrossRefGoogle Scholar
  53. 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):675–679CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2017

Authors and Affiliations

  • Pablo Marcelo Fernández
    • 1
  • María Martha Martorell
    • 2
    Email author
  • Mariana G. Blaser
    • 1
  • Lucas Adolfo Mauro Ruberto
    • 2
    • 3
    • 4
  • Lucía Inés Castellanos de Figueroa
    • 1
    • 5
  • Walter Patricio Mac Cormack
    • 2
    • 3
    • 4
  1. 1.Planta Piloto de Procesos Industriales Microbiológicos (PROIMI-CONICET)San Miguel de TucumánArgentina
  2. 2.Instituto Antártico Argentino (IAA)Buenos AiresArgentina
  3. 3.Universidad de Buenos Aires (UBA)Buenos AiresArgentina
  4. 4.NANOBIOTEC-CONICETBuenos AiresArgentina
  5. 5.Universidad Nacional de Tucumán (UNT)San Miguel de TucumánArgentina

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