Abstract
We surveyed diversity patterns and engaged in bioprospecting for bioactive compounds of fungi associated with the endemic macroalgae, Monostroma hariotii and Pyropia endiviifolia, in Antarctica. A total of 239 fungal isolates were obtained, which were identified to represent 48 taxa and 18 genera using molecular methods. The fungal communities consisted of endemic, indigenous and cold-adapted cosmopolitan taxa, which displayed high diversity and richness, but low dominance indices. The extracts of endemic and cold-adapted fungi displayed biological activities and may represent sources of promising prototype molecules to develop drugs. Our results suggest that macroalgae along the marine Antarctic Peninsula provide additional niches where fungal taxa can survive and coexist with their host in the extreme conditions. We hypothesise that the dynamics of richness and dominance among endemic, indigenous and cold-adapted cosmopolitan fungal taxa might be used to understand and model the influence of climate change on the maritime Antarctic mycota.
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Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLASTand PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
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 Bio Bioch 38:3057–3064
Atalla MM, Zeinab HK, Eman RH, Amani AY, Abeer AAEA (2011) Physiological studies on some biologically active secondary metabolites from marine-derived fungus Penicillium brevicompactum. www.Gate2Biotech.com, 1: 1–15
Bhadury P, Bik H, Lambshead JD, Austen MC, Smerdon GR, Rogers AD (2011) Molecular diversity of fungal phylotypes co-amplified alongside nematodes from coastal and deep-sea marine environments. PLoS ONE 6e26445:1–7
Blanchette RA, Held BW, Arenz BE, Jurgens JA, Baltes NJ et al (2010) An Antarctic hot spot for fungi at Shackleton’s historic hut on Cape Royds. Microb Ecol 60:29–38
Bridge PD, Spooner BM (2012) Non-lichenized Antarctic fungi: transient visitors or members of a cryptic ecosystem? Fungal Ecol 5:381–394
Carvalho CR, Gonçalves VN, Pereira CB, Johann S, Galliza IV et al (2012) The diversity, antimicrobial and anticancer activity of endophytic fungi associated with the medicinal plant Stryphnodendron adstringens (Mart.) Coville (Fabaceae) from the Brazilian savannah. Symbiosis 57:95–107
Charpy-Roubaud C, Sourina A (1990) The comparative estimation of phytoplanktonic, microphytobenthic and macrophytobenthic primary production in the oceans. Mar Microb Food Webs 4:31–57
Clarke A, Murphy EJ, Meredith MP, King JC, Peck LS et al (2007) Climate change and the marine ecosystem of the western Antarctic Peninsula. Phil Trans Royal Soc 362:149–166
Donachie SP, Zdanowski MK (1998) Potential digestive function of bacteria in krill, Euphausia superba stomach. Aquat Microb Ecol 14:129–136
Espinel-Ingroff A, Kerkering TM (1991) Spectrophotometric method of inoculum preparation for the in vitro susceptibility testing of filamentous fungi. J Clin Microbiol 29:393–394
Fell JW, Guého-Kellermann E (2011) Guehomyces Fell & Scorzetti (2004). In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam
Fell JW, Hunter IL (1968) Isolation of heterothallic yeast strains of Metschnikowia Kamienski and their mating reactions with Chlamydozyma Wickerham spp. Anton Leeuw 34:365–376
Fell JW, Hunter IL, Tallman AS (1973) Marine basidiomycetous yeasts (Rhodosporidium spp. n.) with tetrapolar and multiple alletic bipolar mating systems. Can J Microbiol 19:643–657
Fell JW, Statzel AC (1971) Sympodiomycetes gen. n., a yeast-like organism from southern marine waters. Anton Leeuw 37:359–367
Frisvad JC, Samson RA (2004) Polyphasic taxonomy of Penicillium subgenus Penicillium a guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol 49:1–174
Gazis R, Rehner S, Chaverri P (2011) Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol 20:3001–3013
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330
Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya N et al (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME 7:1434–1451
Gonçalves VN, Vaz ABM, Rosa CA, Rosa LH (2012) Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol Ecol 82:459–471
Grasso S, Bruni V, Maio G (1997) Marine fungi in Terra Nova Bay (Ross Sea, Antarctica). Microbiologica 20:371–376
Guiry MD, Guiry GM (2012) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway.http://www.algaebase.org; searched on 11 October 2012
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4:1–9
Harrington TC, McNew DL (2003) Phylogenetic analysis places the phialophora-like anamorph genus Cadophora in the Helotiales. Mycotaxon 87:141–151
Hoog GS de, Guarro J, Gené J, Figueras MA (2000) Atlas of clinical fungi, 2nd edn. Centraalbureau voor Schimmelcultures, Utrecht/Universitat Rovira i Virgili, Reus
Hyde KD, Lee SY (1995) Ecology of mangrove fungi and their role in nutrient cycling. What gaps occur in our knowledge? Hydrobiologia 295:107–118
Iwamoto C, Yamada T, Ito Y, Minoura K, Numata A (2001) Cytotoxic cytochalasans from a Penicillium species separated from a marine alga. Tetrahedron 57:2997–3004
Jones EB (2011) Fifty years of marine mycology. Fungal Div 50:73–112
Jones EBG, Sakayarol J, Suetrong S, Smorithipol S, Pang KL (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Div 35:1–187
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2011) Dictionary of the Fungi, 10th edn. CAB International, Wallingford
Kohlmeyer J, Kohlmeyer E (1979) Marine mycology, the higher fungi. Academic Press.
Kurtzman CP, Fell JW (2011) The yeast, a taxonomic study, 5th edn. Amsterdam, Elsevier
Lachance MA, Bowles JM, Starmer WT, Barker JS (1999) Kodamaea kakaduensis and Candida tolerans, two new ascomycetous yeast species from Australian hibiscus flowers. Can J Microbiol 45:172–177
Li Y, Sun B, Liu S, Jiang L, Liu X, Zhang H, Che Y (2008) Bioactive asterric acid derivatives from the Antarctic ascomycete Fungus Geomyces sp. J Nat Prod 71:1643–1646
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
Lorch JM, Lindner DL, Gargas A, Muller LK, Minnis AM, Blehert DS (2013) A culture-based survey of fungi in soil from bat hibernacula in the eastern United States and its implications for detection of Geomyces destructans, the causal agent of bat white-nose syndrome. Mycologia 105:237–252
Mercantini R, Marsella R, Cervellati MC (1989) Keratinophilic fungi isolated from Antarctic soil. Mycopathologia 106:47–52
Minnis AM, Lindner DL (2013) Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 117:638--649
National Committee for Clinical Laboratory Standards (2003) Methods for dilution antimicrobial susceptibility testes for bacteria that grow aerobically. Approved standard. 5th ed. NCCLS document M11-A5. NCCLS, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087-1898, USA
Nedzarek A, Rakusa-Suszczewski S (2004) Decomposition of macroalgae and the release of nutrients in admiralty Bay, king George island, antarctica. Polar Biosci 17:16–35
Onofri S, Zucconi L, Tosi S (2007) Continental Antarctic fungi. IHW-Verlag, Eching bei München
Parish CA, Cruz M, Smith SK, Zink D, Baxter J et al (2009) Antisense-guided isolation and structure elucidation of pannomycin, a substituted cis-decalin from Geomyces pannorum. J Nat Prod 72:59–62
Quartino ML, Zaixso HE, Boraso de Zaixso AL (2005) Biological and environmental characterization of marine macroalgal assemblages in Potter Cove, South Shetland Islands, Antarctica. Bot Mar 48:187–197
Romanha AJ, de Castro SL, Soeiro MNC, Lannes-Vieira J, Ribeiro I et al (2010) In vitro and in vivo experimental models for drug screening and development for Chagas disease. Mem Inst Oswaldo Cruz 105:233–238
Rosa LH, Vaz ABM, Caligiorne RB, Campolina S, Rosa CA (2009) Endophytic fungi associated with the Antarctic Grass Deschampsia antarctica Desv. (Poaceae). Polar Biol 32:161–167
Rosa LH, Vieira MLA, Santiago IF, Rosa CA (2010) Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol 73:178–189
Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141
Santiago IF, Alves TMA, Rabello A, Sales-Júnior PA, Romanha AJ et al (2012) Leishmanicidal and antitumoral activities of endophytic fungi associated with the Antartic angiosperms Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. Extremophiles 16:95–103
Stchigel AM, Cano J, MacCormack CW (2001) Antarctomyces psychrotrophicus gen. et sp. nov., a new ascomycete from Antarctica. Mycol Res 105:377–382
Suryanarayanan TS, Venkatachalam A, Thirunavukkarasu N, Ravishankar JP, Doble M, Geetha V (2010) Internal mycobiota of marine macroalgae from the Tamilnadu coast: distribution, diversity and biotechnological potential. Bot Mar 53:457–468
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tosi S, Casado B, Gerdol R, Caretta G (2002) Fungi isolated from antarctic mosses. Polar Biol 25:262–268
Vaz ABM, Rosa LH, Vieira MLA, Garcia V, Teixeira LCRS et al (2011) The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in antarctica. Braz J Microbiol 42:937–947
Vishniac HS (2006) Yeast biodiversity in the Antarctic. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer-Verlag, Heidelberg, pp 221–240
Vishniac HS, Kurtzman CP (1992) Cryptococcus antarcticus sp. nov, and Cryptococcus albidosimilis sp. nov, basidioblastomycetes from antarctic soils. Int J Syst Bacteriol 42:547–553
Wedge DE, Kuhajek JM (1998) A microbioassay for fungicide discovery. SAAS Bull Biochem Biotechnol 11:1–7
White TJ, Bruns TD, Lee SB (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis NA, Gelfand J, Sninsky J et al (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Wiencke C, Clayton MN (2002) Antarctic seaweeds. A.R.G. Gantner Verlag KG, Ruggell
Zuccaro A, Mitchell JI (2005) Fungal communities of seaweeds. In: Dighton J, White JFP, Oudemans P (eds) The fungal community: its organization and role in the ecosystem. CRC Press, /Taylor and Francis, Boca Raton, pp 533–579
Zucconi L, Selbmann L, Buzzini P, Turchetti B, Guglielmin M et al (2012) Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol 35:749–757
Acknowledgements
We acknowledge the financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Processes PROANTAR 557030/2009-9, Universal 471721/2013-1 and PROANTAR 407230/2013-0, Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG), Process Universal 0050-13 and the Financiadora de Estudos e Projetos (FINEP 2084/07), the Program for Technological Development of Tools for Health-PDTIS-FIOCRUZ. A.M. Minnis received financial support from the US Forest Service, Northern Research Station and the Inter-Agency Agreement F11RG00184 grant from the US Fish and Wildlife Service. The results of this study are part of the Master Science degree of LE Furbino within the Programa of Pós-Graduação in Biotecnologia of UFOP and the Pos-Doctoral of VM Godinho of CNPq under supervision of LH Rosa.
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Furbino, L.E., Godinho, V.M., Santiago, I.F. et al. Diversity Patterns, Ecology and Biological Activities of Fungal Communities Associated with the Endemic Macroalgae Across the Antarctic Peninsula. Microb Ecol 67, 775–787 (2014). https://doi.org/10.1007/s00248-014-0374-9
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DOI: https://doi.org/10.1007/s00248-014-0374-9