Abstract
The interest in the diversity of yeasts in the Antarctic environment has increased in recent years, mainly because Antarctic microbiology is a recent science, and little is known about the biodiversity and genetic resources of the microorganisms that inhabit this ecosystem. This study aimed to determine the diversity of epiphytic yeasts in samples of Deschampsia antarctica, Colobanthus quitensis, and bryophytes, as well yeasts present in biofilms collected from Antarctic meltwater. Samples were collected in the summer of 2014 and 2015 during expeditions organized by the Brazilian Antarctic Program. A total of 310 yeasts were isolated, and 34 species were identified by sequencing the D1/D2 domains of the rDNA region belonging to 18 genera. The species Vishniacozyma victoriae and Mrakia gelida were the most abundant. Dioszegia antarctica and Leucosporidium creatinivorum were found only in plant substrates. Most psychrophilic yeasts were isolated from biofilms, including Glaciozyma antarctica, Glaciozyma martinii, Mrakia gelida, Mrakia frigida, Mrakia robertii, Phenoliferia glacialis, and Phenoliferia psychrophenolica, suggesting that the substrates examined in this study represented an interesting habitat for the isolation and characterization of epiphytic and non-epiphytic yeasts that colonize the Antarctic region.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Białkowska AM, SzulczewskA KM, 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 Biol 40:1787–1803. https://doi.org/10.1007/s00300-017-2102-7
Bioinformatics & Systems Biology. Team VIB/UGent Bioinformatics & Evolutionary Genomics, Belgium, 2018. http://bioinformatics.psb.ugent.be/publications. Accessed 01 Jun 2018
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 72:354–369. https://doi.org/10.1111/j.1574-6941.20
Brandão LR, Aline BM, Vaz ABM, Lilia C, Santo LC, Pimenta RS, Morais PB, Libkind D, Rosa LH, Rosa CA (2017) Diversity and biogeographical patterns of yeast communities in Antarctic, Patagonian and tropical lakes. Fungal Ecol 28:33–43. https://doi.org/10.1016/j.funeco.2017.04.003
Buzzini P, Turk M, Perini L, Turchetti B, Gunde-Cimerman N (2017) Yeasts in polar and subpolar habitats. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: diversity. Springer, Cham. https://doi.org/10.1007/978-3-319-62683-3_11
Carrasco M, Rozas MJ, 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. https://doi.org/10.1186/1471-2180-12-251
Characklis WG, McFeters GA, Marshall KC (1990) Physiological ecology in biofilm systems. In: Characklis WG, Marshall KC (eds) Biofilms, vol 1. Wiley, New York, pp 341–394
Connell LB, Redman R, Rodriguez R, Barrett A, Iszard M, Fonseca A (2010) Dioszegia antarctica sp. nov. and Dioszegia cryoxerica sp. nov., psychrophilic basidiomycetous yeasts from polar desert soils in Antarctica. Evol Microbiol 60:1466–1472. https://doi.org/10.1099/ijs.0.015412-0
Cowan DA, Tow LA (2004) Endangered Antarctic environments. Ann Rev Microbiol 58:649–690. https://doi.org/10.1146/annurev.micro.57.030502.090811
De Garcia V, Zalar P, Brizzio S, Gunde-Cimerman N, van Broock M (2012) Cryptococcus species (Tremellales) from glacial biomes in the southern (Patagonia) and northern (Svalbard) hemispheres. FEMS Microbiol Ecol 82:523–539. https://doi.org/10.1111/j.1574-6941.2012.01465.x
Duarte AWF, Dayo-Owoyemi I, Nobre FS, Pagnoca FC, Chaud LCS, Pessoa A, Felipe MGA, Sette LD (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
Duarte AWF, Passarini MRZ, Delforno TP, Pelizzari FM, Cipro CVZ, Montene RC, Petry MV, Putzke J, Rosa LH, Sette LD (2016) Yeasts from macroalgae and lichens that inhabit the South Shetland Islands, Antarctica. Env Microbiology 8:874–885. https://doi.org/10.1111/1758-2229.12452
Furbino LE, Godinho VM, Santiago IF, Pellizari FM, Alves TMA, Zani CL, Junior PAS, Romanha AJ, Carvalho AGO, Gil LHVG, Rosa CA, Minnis AM, Rosa LH (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microb Ecol 67:775–787. https://doi.org/10.1007/s00248-014-0374-9
Gadanho M, Almeida JMF, Sampaio JP (2002) Assessment of yeast diversity in a marine environment in the south of Portugal by microsatellite-primed PCR. Antonie Van Leeuwenhoek 84:217–227
Glushakova AM, Chernov IY (2007) Seasonal dynamic of the numbers of epiphytic yeasts. Microbiology 76:590–595. https://doi.org/10.1134/s0026261707050128
Gocheva YG, Krumova ET, Slokoska LS, Miteva JG, Vassilev SV, Angelova MB (2006) Cell response of Antarctic and temperate strains of Penicillium spp. to different growth temperature. Mycol Res 110:1347–1354. https://doi.org/10.1016/j.mycres.2006.08.007
Godinho VM, Furbino L, Santiago I, Pellizari NY, Yokoya NS, Pupo D, Alves M, Junior PAS, Romanha AJ, Zani CL, Cantrell CL, Rosa CA, Rosa LH (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451. https://doi.org/10.1038/ismej.2013.77
Gonçalves VN, Carvalho CR, Johann S, Mendes G, Alves MA, Zani CL, Junior ZPAS, Murta SMF, Romamha AJ, Cantrell CL, Rosa CA, Rosa LH (2015) Antibacterial, antifungal and antiprotozoal activities of fungal communities present in different substrates from Antarctica. Polar Biol 38:1143–1152. https://doi.org/10.1007/s00300-015-1672-5
Isaeva OV, Glushakova AM, Garbuz SA, Kachalkin AV, Chernov IY (2010) Endophytic yeast fungi in plant storage tissues. Biol Bull 37:26–34. https://doi.org/10.1134/S1062359010010048
Janisiewicz WJ, Kurtzman CP, Buyer JS (2010) Yeasts associated with nectarines and their potential for biological control of brown rot. Yeast 27:389–398. https://doi.org/10.1002/yea.1763
Kachalkin AV, Glushakova AM, Yurkov AM, Chernov IY (2008) Characterization of yeast groupings in the phyllosphere of Sphagnum mosses. Microbiology 77:474–481. https://doi.org/10.1134/s0026261708040140
Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73:331–371
Kurtzman CP, Fell JW, Boekhout T (2011) Gene sequence analyses and other DNA-based methods for yeast species recognition. The Yeasts: a Taxonomic Study, 5th edn. In: Kurtzman CP, Fell JW & Boekhout T (eds), Science B.V., Elsevier, Amsterdam, pp 137–144
Lachance MA, Bowles JM, Starmer T, Barker JS (1999) Kodamaea kakaduensis and Candida tolerans, two new ascomycetous yeast species from Australian Hibiscus flowers. Can J Microbiol 45:172–177. https://doi.org/10.1139/w98-225
Libkind D, Brizzio S, Ruffini A, Gadanho M, Broock M, Sampaio JP (2003) Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Antonie Van Leeuwenhoek 84:313–322. https://doi.org/10.1023/A:1026058116545
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
Nilsson RH, Kristansson E, Ryberg M, Hallengerg N, Larsson KH (2008) Intraspecific ITS variability in the Kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evolut Bioinf Online 4:93–201
Oksanen J, Kindt R, Legendre P, O’hara, B, Stevens, M H H 2007. Vegan: Community Ecology Package. R package version 1.8-8
Pavel AB, Vasile CI, PyElph (2012) A software tool for gel images analysis and phylogenetics. BMC Bioinf. https://doi.org/10.1186/1471-2105-13-9
R development core team. 2007. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ruisi S, Barreca D, Selbmann L, ZucconI L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:12–141
Santiago IF, Rosa CA, Rosa LH (2016) Endophytic symbiont yeasts associated with the Antarctic angiosperms Deschampsia antarctica and Colobanthus quitensis. Polar Biol 40:177–183. https://doi.org/10.1007/s00300-016-1940-z
Shivaji S, Prasad GS (2009) Antarctic yeast biotechnology: diversity and applications. In: Satyanarayna T, Kunze (eds) Springer, Berlin, pp 3–16
Singh SM, Nayaka S (2017) Contributions to the floral diversity of Schirmacher Oasis and Larsemann Hills Antarctica. Proc Indian Natn Sci Acad 2:469–481. https://doi.org/10.16943/2017/48957
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tonkova EV, Romanovskaya V, Gladka G, Gouliamova D, Tomova I, Stoilova-Disheya M, Tashyrev O (2014) Ecophysiological properties of cultivable heterotrophic bacteria and yeasts dominating in phytocenoses of Galindez Island, maritime Antarctica. World J Microbiol Biotechnol 30:1387–1398. https://doi.org/10.1007/s11274-013-1555-2
Troncoso E, Barahona S, Carrasco M, Villarreal P, Alcaíno J, Cifuentes V, Baeza M (2016) Identification and characterization of yeasts isolated from the South Shetland Islands and the Antarctic Peninsula. Polar Biol 40:649–658. https://doi.org/10.1007/s00300-016-1988-9
Tsuji M, Kudoh S, Hoshimo T (2016) Ethanol productivity of cryophilic basidiomycetous yeast Mrakia spp. Correlates with ethanol tolerance. Mycoscience 57:42–50. https://doi.org/10.1016/j.myc.2015.08.002
Turchetti B, Buzzini P, Goretti M, Branda E, DiolaiutI G, Agata CD, Smiraglia C, Vaughan-Martini A (2008) Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbiol Ecol 63:73–83. https://doi.org/10.1111/j.1574-6941.2007.00409.x
Vaz ABM, Rosa LH, Vieira MLA, Garcia V, Brandão LR, Teixeira LCRS, Moliné M, Libkind D, Broock MV, Rosa CA (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in antarctica. Braz J Microbiol 42:937–947. https://doi.org/10.1590/S1517-83822011000300012
Vero S, Garmendia G, Gonzalez MB, Bentacur O, Wisniewski M (2013) Evaluation of yeasts obtained from Antarctic soil samples as biocontrol agents for the management of postharvest diseases of apple (Malus X domestica). FEMS Yeast Res 13:189–199. https://doi.org/10.1111/1567-1364.12021
Vishniac HS (2006) A multivariate analysis of soil yeasts isolated from a latitudinal gradient. Microb Ecol 52:90–103. https://doi.org/10.1007/s00248-006-9066-4
Acknowledgments
The authors thank Cristiane Martins Coelho and Marcia Regina Marson Oliveira for their personal collaboration. Financial support from CAPES (Coordenacão de Aperfeiçoamento de Pessoal de Nível Superior) (AUXPEPRÓ-AMAZÔNIA-3312/2013/process n 23038.010315/2013-66), Programa Antártico Brasileiro (Brazilian Antarctic Program; PROANTAR process 407230/2013-0), and INCT Criosfera is acknowledged.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Communicated by L. Huang.
Rights and permissions
About this article
Cite this article
Ferreira, E.M.S., de Sousa, F.M.P., Rosa, L.H. et al. Taxonomy and richness of yeasts associated with angiosperms, bryophytes, and meltwater biofilms collected in the Antarctic Peninsula. Extremophiles 23, 151–159 (2019). https://doi.org/10.1007/s00792-018-1069-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-018-1069-9