Advertisement

Extremophiles

, Volume 20, Issue 5, pp 759–769 | Cite as

Yeasts from sub-Antarctic region: biodiversity, enzymatic activities and their potential as oleaginous microorganisms

  • A. Martinez
  • I. Cavello
  • G. Garmendia
  • C. Rufo
  • S. Cavalitto
  • S. VeroEmail author
Original Paper

Abstract

Various microbial groups are well known to produce a range of extracellular enzymes and other secondary metabolites. However, the occurrence and importance of investment in such activities have received relatively limited attention in studies of Antarctic soil microbiota. Sixty-one yeasts strains were isolated from King George Island, Antarctica which were characterized physiologically and identified at the molecular level using the D1/D2 region of rDNA. Fifty-eight yeasts (belonging to the genera Cryptococcus, Leucosporidiella, Rhodotorula, Guehomyces, Candida, Metschnikowia and Debaryomyces) were screened for extracellular amylolytic, proteolytic, esterasic, pectinolytic, inulolytic xylanolytic and cellulolytic activities at low and moderate temperatures. Esterase activity was the most common enzymatic activity expressed by the yeast isolates regardless the assay temperature and inulinase was the second most common enzymatic activity. No cellulolytic activity was detected. One yeast identified as Guehomyces pullulans (8E) showed significant activity across six of seven enzymes types tested. Twenty-eight yeast isolates were classified as oleaginous, being the isolate 8E the strain that accumulated the highest levels of saponifiable lipids (42 %).

Keywords

Bioenergetics Enzymes Psychrophiles 

Notes

Acknowledgments

This work was supported by grants from Agencia Nacional de Investigación e Innovación (ANII, FSE 102780), Instituto Antártico Uruguayo (IAU), Pedeciba, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 112-201101-00662) and Agencia Nacional de PromociónCientífica y Tecnológica (PICT 2014-1655).

References

  1. Amaretti A, Raimondi S, Sala M, Roncaglia L, De Lucia M, Leonardi A, Rossi M (2010) Single cell oils of the cold-adapted oleaginous yeast Rhodotorula glacialis DBVPG 4785. Microb Cell Fact. doi: 10.1186/1475-2859-9-73 PubMedPubMedCentralGoogle Scholar
  2. Aurilia V, Parracino A, D’Auria S (2008) Microbial carbohydrate esterases in cold adapted environments. Gene 410:234–240. doi: 10.1016/j.gene.2007.12.019 CrossRefPubMedGoogle Scholar
  3. Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369CrossRefPubMedGoogle Scholar
  4. Buzzini P, Margesin R (2014) Cold-adapted yeasts: a lesson from the cold and a challenge for the XXI century. Coldadapt Yeasts Biodivers Adapt Strateg Biotechnol Signif 9783642396816:3–22. doi: 10.1007/978-3-642-39681-6_1 CrossRefGoogle Scholar
  5. 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. doi: 10.1046/j.1365-2672.2002.01783.x CrossRefPubMedGoogle Scholar
  6. 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. doi: 10.1186/1471-2180-12-251 PubMedPubMedCentralGoogle Scholar
  7. Chang CF, Lee CF, Liu SM (2008) Cryptococcus keelungensis sp. nov., an anamorphic basidiomycetous yeast isolated from the sea-surface microlayer of the north-east coast of Taiwan. Int J Syst Evol Microbiol 58:2973–2976. doi: 10.1099/ijs.0.65773-0 CrossRefPubMedGoogle Scholar
  8. Chang CF, Lee CF, Lin KY, Liu SM (2016) Diversity of yeasts associated with the sea surface microlayer and underlying water along the northern coast of Taiwan. Res Microbiol 167:35–45. doi: 10.1016/j.resmic.2015.08.005 CrossRefPubMedGoogle Scholar
  9. Connell L, Redman R, Craig S, Rodriguez R (2006) Distribution and abundance of fungi in the soils of Taylor Valley. Antarct Soil Biol Biochem 38:3083–3094. doi: 10.1016/j.soilbio.2006.02.016 CrossRefGoogle Scholar
  10. Connell LB, Redman R, Rodriguez R, Barrett A, Iszard M, Fonseca Á (2010) Dioszegia antarctica sp. nov. and Dioszegia cryoxerica sp. nov., psychrophilic basidiomycetous yeasts from polar desert soils in Antarctica. Int J Syst Evol Microbiol 60:1466–1472. doi: 10.1099/ijs.0.015412-0 CrossRefPubMedGoogle Scholar
  11. De García V, Brizzio S, Libkind D, Buzzini P, Van Broock M (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia. Argent FEMS Microbiol Ecol 59:331–341. doi: 10.1111/j.1574-6941.2006.00239.x CrossRefGoogle Scholar
  12. Di Menna ME (1966) Yeasts in Antarctic soils. Antonie van Leeuwenhoek 32:29–38CrossRefPubMedGoogle Scholar
  13. Di Rienzo JACF, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2009) InfoStat versión 2009. Universidad Nacional de Córdoba, ArgentinaGoogle Scholar
  14. Duarte AWF et al (2013) Taxonomic assessment and enzymes production by yeasts isolated from marine and terrestrial Antarctic samples. Extremophiles 17:1023–1035. doi: 10.1007/s00792-013-0584-y CrossRefPubMedGoogle Scholar
  15. Fell JW, Mrakia Y (2011) Yamada & Komagata (1987). Yeasts 3:1503–1510. doi: 10.1016/b978-0-444-52149-1.00123-3 CrossRefGoogle Scholar
  16. Fonseca A, Scorzetti G, Fell JW (2000) Diversity in the yeast Cryptococcus albidus and related species as revealed by ribosomal DNA sequence analysis. Can J Microbiol 46:7–27CrossRefPubMedGoogle Scholar
  17. Frisvad JC (2008) Fungi in cold ecosystems. In: Psychrophiles: from biodiversity to biotechnology, pp 137–156. doi: 10.1007/978-3-540-74335-4_9
  18. Garay LA et al (2016) Eighteen new oleaginous yeast species. J Ind Microbiol Biotechnol: 1–14Google Scholar
  19. Godinho VM et al (2015) Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 19:585–596. doi: 10.1007/s00792-015-0741-6 CrossRefPubMedGoogle Scholar
  20. Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis Palaeontol Electron 4:XIX–XXGoogle Scholar
  21. Kimura K, Yamaoka M, Kamisaka Y (2004) Rapid estimation of lipids in oleaginous fungi and yeasts using Nile red fluorescence. J Microbiol Methods 56:331–338. doi: 10.1016/j.mimet.2003.10.018 CrossRefPubMedGoogle Scholar
  22. Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361. doi: 10.1016/j.resmic.2010.12.004 CrossRefPubMedGoogle Scholar
  23. Margesin R, Fonteyne PA, Schinner F, Sampaio JP (2007) Rhodotorula psychrophila sp. nov., Rhodotorula psychrophenolica sp. nov. and Rhodotorula glacialis sp. nov., novel psychrophilic basidiomycetous yeast species isolated from alpine environments. Int J Syst Evol Microbiol 57:2179–2184. doi: 10.1099/ijs.0.65111-0 CrossRefPubMedGoogle Scholar
  24. Mohamed Hatha AA, Rahiman Mujeeb RK, Krishnan KP, Saramma AV, Saritha G, Lal D (2013) Characterisation and bioprospecting of cold adapted yeast from water samples of Kongsfjord. Nor Arct Indian J Mar Sci 42:458–465Google Scholar
  25. Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167PubMedPubMedCentralGoogle Scholar
  26. Nakagawa T, Ikehata R, Uchino M, Miyaji T, Takano K, Tomizuka N (2006) Cold-active acid β-galactosidase activity of isolated psychrophilic-basidiomycetous yeast Guehomyces pullulans. Microbiol Res 161:75–79CrossRefPubMedGoogle Scholar
  27. Pereyra V, Martinez A, Rufo C, Vero S (2014) Oleaginous yeasts form Uruguay and Antarctica as renewable raw material for biodiesel production. Am J Biosci 2:251–257CrossRefGoogle Scholar
  28. Pulicherla K, Ghosh M, Kumar PS, Rao KS (2012) Psychrozymes—the next generation industrial enzymes. J Mar Sci Res Dev 2011Google Scholar
  29. Quesada A, Vincent W (1997) Strategies of adaptation by Antarctic cyanobacteria to ultraviolet radiation. Eur J Phycol 32:335–342CrossRefGoogle Scholar
  30. Ratledge C, Hall MJ (1979) Accumulation of lipid by Rhodotorula glutinis in continuous culture. Biotechnol Lett 1:115–120. doi: 10.1007/bf01386709 CrossRefGoogle Scholar
  31. Renker C, Blanke V, Börstler B, Heinrichs J, Buscot F (2004) Diversity of Cryptococcus and Dioszegia yeasts (Basidiomycota) inhabiting arbuscular mycorrhizal roots or spores. FEMS Yeast Res 4:597–603CrossRefPubMedGoogle Scholar
  32. Rossi M et al (2009) Growth, lipid accumulation, and fatty acid composition in obligate psychrophilic, facultative psychrophilic, and mesophilic yeasts. FEMS Microbiol Ecol 69:363–372. doi: 10.1111/j.1574-6941.2009.00727.x CrossRefPubMedGoogle Scholar
  33. Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Bio/Technol 6:127–141CrossRefGoogle Scholar
  34. Schena L, Ippolito A, Zahavi T, Cohen L, Nigro F, Droby S (1999) Genetic diversity and biocontrol activity of Aureobasidium pullulans isolates against postharvest rots. Postharvest Biol Technol 17:189–199CrossRefGoogle Scholar
  35. Shivaji S, Prasad G (2009) Antarctic yeasts: biodiversity and potential applications. In: Yeast biotechnology: diversity and applications. Springer, New York, pp 3–18Google Scholar
  36. Sitepu IR et al (2012) An improved high-throughput Nile red fluorescence assay for estimating intracellular lipids in a variety of yeast species. J Microbiol Methods 91:321–328. doi: 10.1016/j.mimet.2012.09.001 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sitepu IR et al (2013) Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Bioresour Technol 144:360–369. doi: 10.1016/j.biortech.2013.06.047 CrossRefPubMedGoogle Scholar
  38. Sitepu IR, Garay LA, Sestric R, Levin D, Block DE, German JB, Boundy-Mills KL (2014) Oleaginous yeasts for biodiesel: current and future trends in biology and production. Biotechnol Adv 32:1336–1360. doi: 10.1016/j.biotechadv.2014.08.003 CrossRefPubMedGoogle Scholar
  39. Sláviková E, Košíková B, Mikulášová M (2002) Biotransformation of waste lignin products by the soil-inhabiting yeast Trichosporon pullulans. Can J Microbiol 48:200–203CrossRefPubMedGoogle Scholar
  40. Thakur MS, Prapulla SG, Karanth NG (1989) Estimation of intracellular lipids by the measurement of absorbance of yeast cells stained with Sudan Black B. Enzyme Microb Technol 11:252–254CrossRefGoogle Scholar
  41. Tin T, Fleming ZL, Hugh KA, Ainley DG, Convey P, Morenos CA, Pfeiffer S, Scott J, Snape I (2009) Impacts of local human activities on the Antarctic environment. Antarc Sci 21:3–33CrossRefGoogle Scholar
  42. Turchetti B et al (2011) Psychrophilic yeasts from Antarctica and European glaciers: description of Glaciozyma gen. nov., Glaciozyma martinii sp. nov. and Glaciozyma watsonii sp. nov. Extremophiles 15:573–586. doi: 10.1007/s00792-011-0388-x CrossRefPubMedGoogle Scholar
  43. Vincent WF (2000) Evolutionary origins of Antarctic microbiota: invasion, selection and endemism. Antarct Sci 12:374–385CrossRefGoogle Scholar
  44. Vishniac HS (2006a) A multivariate analysis of soil yeasts isolated from a latitudinal gradient. Microb Ecol 52:90–103. doi: 10.1007/s00248-006-9066-4 CrossRefPubMedGoogle Scholar
  45. Vishniac HS (2006) Yeast biodiversity in the Antarctic. In: Biodiversity and ecophysiology of yeasts. Springer, New York, pp 419–440Google Scholar
  46. Vorapreeda T, Thammarongtham C, Cheevadhanarak S, Laoteng K (2012) Alternative routes of acetyl-CoA synthesis identified by comparative genomic analysis: involvement in the lipid production of oleaginous yeast and fungi. Microbiology 158:217–228CrossRefPubMedGoogle Scholar
  47. Zhang S, Skerker JM, Rutter CD, Maurer MJ, Arkin AP, Rao CV (2015) Engineering Rhodosporidium toruloides for increased lipid production. Biotechnol BioengGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  • A. Martinez
    • 1
  • I. Cavello
    • 2
  • G. Garmendia
    • 1
  • C. Rufo
    • 3
  • S. Cavalitto
    • 2
  • S. Vero
    • 1
    Email author
  1. 1.Cátedra de Microbiología, Departamento de Biociencias, Facultad de QuímicaUniversidad de la RepúblicaMontevideoUruguay
  2. 2.Research and Development Center for Industrial FermentationsCINDEFI (CONICET, La Plata, UNLP)La PlataArgentina
  3. 3.Facultad de Química, Instituto Polo TecnológicoUniversidad de la RepúblicaPandoUruguay

Personalised recommendations