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Microbial Ecology

, Volume 77, Issue 1, pp 12–24 | Cite as

Fungi from Admiralty Bay (King George Island, Antarctica) Soils and Marine Sediments

  • Lia Costa Pinto Wentzel
  • Fábio José Inforsato
  • Quimi Vidaurre Montoya
  • Bruna Gomes Rossin
  • Nadia Regina Nascimento
  • André Rodrigues
  • Lara Durães Sette
Fungal Microbiology

Abstract

Extreme environments such as the Antarctic can lead to the discovery of new microbial taxa, as well as to new microbial-derived natural products. Considering that little is known yet about the diversity and the genetic resources present in these habitats, the main objective of this study was to evaluate the fungal communities from extreme environments collected at Aldmiralty Bay (Antarctica). A total of 891 and 226 isolates was obtained from soil and marine sediment samples, respectively. The most abundant isolates from soil samples were representatives of the genera Leucosporidium, Pseudogymnoascus, and a non-identified Ascomycota NIA6. Metschnikowia sp. was the most abundant taxon from marine samples, followed by isolates from the genera Penicillium and Pseudogymnoascus. Many of the genera were exclusive in marine sediment or terrestrial samples. However, representatives of eight genera were found in both types of samples. Data from non-metric multidimensional scaling showed that each sampling site is unique in their physical-chemical composition and fungal community. Biotechnological potential in relation to enzymatic production at low/moderate temperatures was also investigated. Ligninolytic enzymes were produced by few isolates from root-associated soil. Among the fungi isolated from marine sediments, 16 yeasts and nine fungi showed lipase activity and three yeasts and six filamentous fungi protease activity. The present study permitted increasing our knowledge on the diversity of fungi that inhabit the Antarctic, finding genera that have never been reported in this environment before and discovering putative new species of fungi.

Keywords

Extremophiles Fungal diversity Marine mycology Maritime Antarctica Cold-adapted enzymes 

Notes

Funding Information

This paper was supported by grants financed by FAPESP (reference numbers: #2013/19486-0 and #2016/07957-7), and by scholarships financed by CAPES. LDS and AR thank the National Council for Scientific and Technological Development (CNPq) for Productivity Fellowships 304103/2013-6 and 305341/2015-4. LDS thanks MICROSFERA project (PROANTAR/CNPq) for the support with sample collection.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1217_MOESM1_ESM.docx (927 kb)
ESM 1 (DOCX 926 kb)

References

  1. 1.
    Feller G (2013) Psychrophilic enzymes: from folding to function and biotechnology. Scientifica 2013:512840–512828.  https://doi.org/10.1155/2013/512840 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Shivaji S, Prasad GS (2009) Antarctic yeasts: biodiversity and potential applications. In: Yeast biotechnology: diversity and applications. pp 3–18Google Scholar
  3. 3.
    Singh J, Dubey AK, Singh RP (2011) Antarctic terrestrial ecosystem and role of pigments in enhanced UV-B radiations. Rev Environ Sci Biotechnol 10:63–77CrossRefGoogle Scholar
  4. 4.
    Berlemont R, Pipers D, Delsaute M, Angiono F, Feller G, Galleni M, Power P (2011) Exploring the Antarctic soil metagenome as a source of novel cold-adapted enzymes and genetic mobile elements. Rev Argent Microbiol 43:94–103.  https://doi.org/10.1590/S0325-75412011000200005 CrossRefPubMedGoogle Scholar
  5. 5.
    Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci 106:19964–19969.  https://doi.org/10.1073/pnas.0908274106 CrossRefPubMedGoogle Scholar
  6. 6.
    Wynn-Williams DD (1996) Antarctic microbial diversity: the basis of polar ecosystem processes. Biodivers Conserv 5:1271–1293.  https://doi.org/10.1007/BF00051979 CrossRefGoogle Scholar
  7. 7.
    D’Elia T, Veerapaneni R, Theraisnathan V, Rogers S (2009) Isolation of fungi from Lake Vostok accretion ice. Mycologia 101:751–763CrossRefGoogle Scholar
  8. 8.
    Onofri S, Selbmann L, Zucconi L, Pagano S (2004) Antarctic microfungi as models for exobiology. Planet Space Sci 52:229–237.  https://doi.org/10.1016/j.pss.2003.08.019 CrossRefGoogle Scholar
  9. 9.
    Yergeau E, Kowalchuk GA (2008) Responses of Antarctic soil microbial communities and associated functions to temperature and freeze-thaw cycle frequency. Environ Microbiol 10:2223–2235.  https://doi.org/10.1111/j.1462-2920.2008.01644.x CrossRefPubMedGoogle Scholar
  10. 10.
    Vaz ABM, Rosa LH, Vieira MLA, Garcia V, Brandão LR, Teixeira LCRS, 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.  https://doi.org/10.1590/S1517-83822011000300012 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Georlette D, Blaise V, Collins T, D'Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C (2004) Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 28:25–42.  https://doi.org/10.1016/j.femsre.2003.07.003 CrossRefGoogle Scholar
  12. 12.
    Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433.  https://doi.org/10.1146/annurev.biochem.75.103004.142723 CrossRefGoogle Scholar
  13. 13.
    Maciel MJM, Castro e Silva A, Ribeiro HCT (2010) Industrial and biotechnological applications of ligninolytic enzymes of the basidiomycota: a review. Electron J Biotechnol 13:1–13.  https://doi.org/10.2225/vol13-issue6-fulltext-2 CrossRefGoogle Scholar
  14. 14.
    Pannu JS, Kapoor RK (2014) Microbial laccases: a mini-review on their production, purification and applications. Int J Pharm Arch 3:528–536Google Scholar
  15. 15.
    Viswanath B, Rajesh B, Janardhan A et al (2014) Fungal laccases and their applications in bioremediation. Enzyme Res.  https://doi.org/10.1155/2014/163242
  16. 16.
    Cotârleţ M, Negoiţǎ TGH, Bahrim GE, Stougaard P (2011) Partial characterization of cold active amylases and proteases of Streptomyces sp from Antarctica. Braz J Microbiol 42:868–877.  https://doi.org/10.1590/S1517-83822011000300005 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Damaso MCT, Passianoto MA, De Freitas SC et al (2008) Utilization of agroindustrial residues for lipase production by solid-state fermentation. Braz J Microbiol 39:676–681.  https://doi.org/10.1590/S1517-83822008000400015 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Duarte AWF, dos Santos JA, Vianna MV et al (2017) Cold-adapted enzymes produced by fungi from terrestrial and marine Antarctic environments. Crit Rev Biotechnol 38:600–619 1–20CrossRefGoogle Scholar
  19. 19.
    Camargo O, Moniz A, Jorge J, Valadares J (2009) Métodos de Análise Química, Mineralógica e Física dos Solos do Instituto Agronômico de Campinas. In: Boletim Técnico 106. Campinas, pp 47–50Google Scholar
  20. 20.
    Mehra O, Jackson M (1960) Iron oxide removal from soils and clays by a dithionite-citrate system buffered with sodium bicarbonate. In: National Conference on Clays and Clays Minerals, 7, Washington, D.C. Pergamon Press, pp 317–327Google Scholar
  21. 21.
    McKeague JA, Day JH (1966) Dithionite- and oxalate-extractable Fe and Al as aids in differentiating various classes of soils. Can J Soil Sci 46:13–22.  https://doi.org/10.4141/cjss66-003 CrossRefGoogle Scholar
  22. 22.
    McKeague JA, Brydon JE, Miles NM (1971) Differentiation of forms of extractable iron and aluminum in soils1. Soil Sci Soc Am J 35:33.  https://doi.org/10.2136/sssaj1971.03615995003500010016x CrossRefGoogle Scholar
  23. 23.
    Savitha J, Srividya S, Jagat R et al (2007) Identification of potential fungal strain(s) for the production of inducible, extracellular and alkalophilic lipase. Afr J Biotechnol 6:564–568Google Scholar
  24. 24.
    Lacerda LT, Gusmão LFP, Rodrigues A (2018) Diversity of endophytic fungi in Eucalyptus microcorys assessed by complementary isolation methods. Mycol Prog 17:1–9.  https://doi.org/10.1007/s11557-018-1385-6 CrossRefGoogle Scholar
  25. 25.
    Gelfand D, Sninsky J, White T (1990) PCR protocols: a guide to methods and applications. Academic Press, New YorkGoogle Scholar
  26. 26.
    Sampaio JP, Gadanho M, Santos S et al (2001) Polyphasic taxonomy of the basidiomycetous yeast genus Rhodosporidium: Rhodosporidium kratochvilovae and related anamorphic species. Int J Syst Evol Microbiol 51:687–697.  https://doi.org/10.1099/00207713-51-2-687 CrossRefPubMedGoogle Scholar
  27. 27.
    De Almeida JMGCF (2005) Yeast community survey in the Tagus estuary. FEMS Microbiol Ecol 53:295–303.  https://doi.org/10.1016/j.femsec.2005.01.006 CrossRefPubMedGoogle Scholar
  28. 28.
    Duarte AWF, Dayo-Owoyemi I, Nobre FS, Pagnocca 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 CrossRefPubMedGoogle Scholar
  29. 29.
    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, Int J Gen Mol Microbiol 73:331–371.  https://doi.org/10.1023/A:1001761008817 CrossRefGoogle Scholar
  30. 30.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  31. 31.
    Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780.  https://doi.org/10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  33. 33.
    Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120.  https://doi.org/10.1007/BF01731581 CrossRefPubMedGoogle Scholar
  34. 34.
    Hammer Ø, Harper DATAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9.  https://doi.org/10.1016/j.bcp.2008.05.025 CrossRefGoogle Scholar
  35. 35.
    Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9 and earlier. User’s Guide and application. http://purl.oclc.org/estimates
  36. 36.
    Verma AK, Raghukumar C, Verma P, Shouche YS, Naik CG (2010) Four marine-derived fungi for bioremediation of raw textile mill effluents. Biodegradation 21:217–233.  https://doi.org/10.1007/s10532-009-9295-6 CrossRefPubMedGoogle Scholar
  37. 37.
    Kouker G, Jaeger KE (1987) Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol 53:211–213PubMedPubMedCentralGoogle Scholar
  38. 38.
    Arora DS, Gill PK (2001) Comparison of two assay procedures for lignin peroxidase. Enzym Microb Technol 28:602–605.  https://doi.org/10.1016/S0141-0229(01)00302-7 CrossRefGoogle Scholar
  39. 39.
    Wariishi H, Valli K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium: kinetic mechanism and role of chelators. J Biol Chem 267:23688–23695.  https://doi.org/10.1006/abbi.1998.0602 CrossRefPubMedGoogle Scholar
  40. 40.
    Buswell JA, Cai Y, Chang S (1995) Effect of nutrient nitrogen on manganese peroxidase and lacase production by Lentinula (Lentinus) edodes. FEMS Microbiol Lett 128:81–87CrossRefGoogle Scholar
  41. 41.
    Yang J, Koga Y, Nakano H, Yamane T (2002) Modifying the chain-length selectivity of the lipase from Burkholderia cepacia KWI-56 through in vitro combinatorial mutagenesis in the substrate-binding site. Protein Eng 15:147–152.  https://doi.org/10.1093/protein/15.2.147 CrossRefPubMedGoogle Scholar
  42. 42.
    Charney J, Tomarelli RM (1947) A colorimetric method for the determination of the proteolytic activity of duodenal juice. J Biol Chem 171:501–505PubMedGoogle Scholar
  43. 43.
    Costa R, Götz M, Mrotzek N et al (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249.  https://doi.org/10.1111/j.1574-6941.2005.00026.x CrossRefPubMedGoogle Scholar
  44. 44.
    Berríos G, Cabrera G, Gidekel M, Gutiérrez-Moraga A (2013) Characterization of a novel antarctic plant growth-promoting bacterial strain and its interaction with antarctic hair grass (Deschampsia antarctica Desv). Polar Biol 36:349–362.  https://doi.org/10.1007/s00300-012-1264-6 CrossRefGoogle Scholar
  45. 45.
    Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141.  https://doi.org/10.1007/s11157-006-9107-y CrossRefGoogle Scholar
  46. 46.
    Carrasco M, Rozas J, 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.  https://doi.org/10.1186/1471-2180-12-251 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya NS, Pupo D, Alves TMA, S Junior PA, 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 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Loque CP, Medeiros AO, Pellizzari FM, Oliveira EC, Rosa CA, Rosa LH (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648.  https://doi.org/10.1007/S00300-009-0740-0 CrossRefGoogle Scholar
  49. 49.
    Sampaio J (2011) Leucosporidium Fell, Statzell, I. L. Hunter-Phaff (1969). In: Kurtzman CP, Fell J, Boekhout (eds) The yeasts: a taxonomic study, v. 3, part. Elsevier, Amsterdam, pp 1485–1494CrossRefGoogle Scholar
  50. 50.
    Hayes MA (2012) The Geomyces fungi: ecology and distribution. Bioscience 62:819–823.  https://doi.org/10.1525/bio.2012.62.9.7 CrossRefGoogle Scholar
  51. 51.
    Arenz BE, Held BW, Jurgens JA, Farrell RL, Blanchette RA (2006) Fungal diversity in soils and historic wood from the Ross Sea region of Antarctica. Soil Biol Biochem 38:3057–3064.  https://doi.org/10.1016/j.soilbio.2006.01.016 CrossRefGoogle Scholar
  52. 52.
    McRae CF, Seppelt RD, Hocking AD (1999) Penicillium species from terrestrial habitats in the Windmill Islands, East Antarctica, including a new species, Penicillium antarcticum. Polar Biol 21:97–111.  https://doi.org/10.1007/s003000050340 CrossRefGoogle Scholar
  53. 53.
    Crous PW, Braun U, Schubert K, Groenewald JZ (2007) Delimiting Cladosporium from morphologically similar genera. Stud Mycol 58:33–56.  https://doi.org/10.3114/sim.2007.58.02 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Cruywagen EM, Crous PW, Roux J, Slippers B, Wingfield MJ (2015) Fungi associated with black mould on baobab trees in southern Africa. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 108:85–95.  https://doi.org/10.1007/s10482-015-0466-7 CrossRefGoogle Scholar
  55. 55.
    Piñar G, Sterflinger K, Pinzari F (2015) Unmasking the measles-like parchment discoloration: molecular and microanalytical approach. Environ Microbiol 17:427–443.  https://doi.org/10.1111/1462-2920.12471 CrossRefPubMedGoogle Scholar
  56. 56.
    Sandoval-Denis M, Sutton DA, Martin-Vicente A, Cano-Lira JF, Wiederhold N, Guarro J, Gené J (2015) Cladosporium species recovered from clinical samples in the United States. J Clin Microbiol 53:2990–3000.  https://doi.org/10.1128/JCM.01482-15 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Zhang E, Tanaka T, Tajima M, Tsuboi R, Nishikawa A, Sugita T (2011) Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol 55:625–632.  https://doi.org/10.1111/j.1348-0421.2011.00364.x CrossRefPubMedGoogle Scholar
  58. 58.
    Rossman AY, Allen WC, Castlebury LA (2016) New combinations of plant-associated fungi resulting from the change to one name for fungi. IMA Fungus 7:1–7.  https://doi.org/10.5598/imafungus.2016.07.01.01 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Bonugli-Santos R, Passarini C, Rodrigues M et al (2009) Avaliação do potencial biosurfactante de fungos filamentosos associados a cnidários marinhos com atividade de degradação de HPAs. Microbiol Foco 7:12–16Google Scholar
  60. 60.
    Budziszewska J, Szypula W, Wilk M, Wrzosek M (2011) Paraconiothyrium babiogorense sp nov., a new endophyte from fir club moss Huperzia selago (Huperziaceae). Mycotaxon 115:457–468.  https://doi.org/10.5248/115.457 CrossRefGoogle Scholar
  61. 61.
    Crous PW, Wingfield MJ, Guarro J, Cheewangkoon R, van der Bank M, Swart WJ, Stchigel AM, Cano-Lira JF, Roux J, Madrid H, Damm U, Wood AR, Shuttleworth LA, Hodges CS, Munster M, de Jesús Yáñez-Morales M, Zúñiga-Estrada L, Cruywagen EM, de Hoog GS, Silvera C, Najafzadeh J, Davison EM, Davison PJN, Barrett MD, Barrett RL, Manamgoda DS, Minnis AM, Kleczewski NM, Flory SL, Castlebury LA, Clay K, Hyde KD, Maússe-Sitoe SND, Chen S, Lechat C, Hairaud M, Lesage-Meessen L, Pawłowska J, Wilk M, Śliwińska-Wyrzychowska A, Mętrak M, Wrzosek M, Pavlic-Zupanc D, Maleme HM, Slippers B, Mac Cormack WP, Archuby DI, Grünwald NJ, Tellería MT, Dueñas M, Martín MP, Marincowitz S, de Beer ZW, Perez CA, Gené J, Marin-Felix Y, Groenewald JZ (2013) Fungal planet description sheets: 154 – 213. Persoonia 31:188–296.  https://doi.org/10.3767/003158513X675925 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Gomes NGM, Lefranc F, Kijjoa A, Kiss R (2015) Can some marine-derived fungal metabolites become actual anticancer agents? Mar Drugs 13:3950–3991.  https://doi.org/10.3390/md13063950 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Verkley GJM, Da Silva M, Wicklow DT, Crous PW (2004) Paraconiothyrium, a new genus to accommodate the mycoparasite Coniothyrium minitans, anamorphs of Paraphaeosphaeria, and four new species. Stud Mycol 50:323–335Google Scholar
  64. 64.
    Upson R, Newsham KK, Bridge PD, Pearce DA, Read DJ (2009) Taxonomic affinities of dark septate root endophytes of Colobanthus quitensis and Deschampsia antarctica, the two native Antarctic vascular plant species. Fungal Ecol 2:184–196.  https://doi.org/10.1016/j.funeco.2009.02.004 CrossRefGoogle Scholar
  65. 65.
    Gonçalves VN, Carvalho CR, Johann S, Mendes G, Alves TMA, Zani CL, Junior PAS, Murta SMF, Romanha 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 CrossRefGoogle Scholar
  66. 66.
    Haichar FEZ, Marol C, Berge O et al (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230.  https://doi.org/10.1038/ismej.2008.80 CrossRefPubMedGoogle Scholar
  67. 67.
    Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257.  https://doi.org/10.1007/s11104-008-9814-y CrossRefGoogle Scholar
  68. 68.
    Teixeira LCRS, Yeargeau E, Balieiro FC et al (2013) Plant and bird presence strongly influences the microbial communities in soils of Admiralty Bay, Maritime Antarctica. PLoS One 8:e66109.  https://doi.org/10.1371/journal.pone.0066109 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Dennis PG, Rushton SP, Newsham KK, Lauducina VA, Ord VJ, Daniell TJ, O'Donnell AG, Hopkins DW (2012) Soil fungal community composition does not alter along a latitudinal gradient through the maritime and sub-Antarctic. Fungal Ecol 5:403–408.  https://doi.org/10.1016/j.funeco.2011.12.002 CrossRefGoogle Scholar
  70. 70.
    Vishniac HS (1996) Biodiversity of yeasts and filamentous microfungi in terrestrial Antarctic ecosystems. Biodivers Conserv 5:1365–1378.  https://doi.org/10.1007/BF00051983 CrossRefGoogle Scholar
  71. 71.
    Duarte AWF (2014) Biodiversidade de leveduras derivadas de ecossistemas Antárticos marinhos e terrestres e prospecção de lipases. Universidade de São PauloGoogle Scholar
  72. 72.
    Vakhlu J, Kour A (2006) Yeast lipases: enzyme purification, biochemical properties and gene cloning. Electron J Biotechnol 9:69–85CrossRefGoogle Scholar
  73. 73.
    Vaca I, Faúndez C, Maza F, Paillavil B, Hernández V, Acosta F, Levicán G, Martínez C, Chávez R (2013) Cultivable psychrotolerant yeasts associated with Antarctic marine sponges. World J Microbiol Biotechnol 29:183–189.  https://doi.org/10.1007/s11274-012-1159-2 CrossRefPubMedGoogle Scholar
  74. 74.
    Chaturvedi V, Springer DJ, Behr MJ, Ramani R, Li X, Peck MK, Ren P, Bopp DJ, Wood B, Samsonoff WA, Butchkoski CM, Hicks AC, Stone WB, Rudd RJ, Chaturvedi S (2010) Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PLoS One 5:e10783.  https://doi.org/10.1371/journal.pone.0010783 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Edgington S, Thompson E, Moore D, Hughes KA, Bridge P (2014) Investigating the insecticidal potential of Geomyces (Myxotrichaceae: Helotiales) and Mortierella (Mortierellacea: Mortierellales) isolated from Antarctica. Springerplus 3:289.  https://doi.org/10.1186/2193-1801-3-289 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Krishnan A, Alias SA, Wong CMVL, Pang KL, Convey P (2011) Extracellular hydrolase enzyme production by soil fungi from King George Island, Antarctica. Polar Biol 34:1535–1542.  https://doi.org/10.1007/s00300-011-1012-3 CrossRefGoogle Scholar
  77. 77.
    Santos W, Nascimento T, Maciel A, et al (2015) A rapid screening of significative variables in the production of proteases and amylases by submerged fermentation of Geomyces pannorum S2B. In: Anais do XXVIII Congresso Brasileiro de Microbiologia. FlorianópolisGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Lia Costa Pinto Wentzel
    • 1
  • Fábio José Inforsato
    • 1
  • Quimi Vidaurre Montoya
    • 1
  • Bruna Gomes Rossin
    • 2
  • Nadia Regina Nascimento
    • 2
  • André Rodrigues
    • 1
  • Lara Durães Sette
    • 1
  1. 1.Instituto de Biociências, Departamento de Bioquímica e MicrobiologiaSão Paulo State University (UNESP)Rio ClaroBrazil
  2. 2.Instituto de Geociências e Ciências Exatas, Departamento de Planejamento Territorial e GeoprocessamentoSão Paulo State University (UNESP)Rio ClaroBrazil

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