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Antibacterial, antifungal and antiprotozoal activities of fungal communities present in different substrates from Antarctica

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Abstract

Antarctica is a pristine and extreme environment that represents a unique opportunity for taxonomic, ecological and biotechnological studies of the microorganisms. In the present work, the fungal communities of rhizosphere soil of Deschampsia antarctica, soil, ornithogenic soil, marine and lake sediments in the Antarctic Peninsula were characterized as well as their capability to produce bioactive compounds. One hundred fungal isolates were recovered and identified by molecular analysis in 35 different taxa of 20 genera. Pseudogymnoascus sp. 1 and 3, Penicillium sp., Peniophora sp. and Mortierella alpina were the most frequent taxa identified. All isolates were cultured to produce ethanolic extracts, which were assayed against different target organisms to detect antimicrobial (against Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa, Candida albicans, Candida krusei, Cladosporium sphaerospermum and Paracoccidioides brasiliensis), cytotoxic (against breast MCF-7 and renal TK-10 human tumoral cells) and antiprotozoal (against Leishmania amazonensis and Trypanosoma cruzi) activities. Among the three human pathogenic fungal species, 20 extracts showed moderate to high and selective antifungal activity against P. brasiliensis. The extract of Purpureocillium lilacinum displayed high trypanocidal, antifungal and antibacterial activities, but with moderate toxicity over normal cells. Proton nuclear magnetic resonance (1H NMR) spectral analysis indicated the presence of compounds containing a highly functionalized aromatic ring system. Our results suggest that the Antarctic ecosystems represent an interesting habitat for the isolation and characterization of fungal taxa capable to producing bioactive compounds. The fungus P. lilacinum showed strong trypanocidal and antimicrobial activities with moderate toxicity over normal cells, which might be used as scaffold for the development of new drugs.

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References

  • Adams BJ, Bardgett RD, Ayres E, Wall DH, Aislabie J, Bamforth S, Bargagli R, Cary C, Cavacini P, Connell L, Convey P, Fell JW, Frati F, Hogg ID, Newsham KK, O’Donnell A, Russell N, Seppelt RD, Stevens MI (2006) Diversity and distribution of Victoria Land biota. Soil Biol Biochem 38:3003–3018

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bridge PD, Newsham KK (2009) Soil fungal community composition at Mars Oasis, a southern maritime Antarctic site, assessed by PCR amplification and cloning. Fungal Ecol 2:66–74

    Article  Google Scholar 

  • Brunati M, Rojas JL, SpongaF CiciliatoI, Losi D, Elke Göttlich E, de Hoog S, Genilloud O, Marinelli F (2009) Diversity and pharmaceutical screening of fungi from benthic mats of Antarctic lakes. Mar Genomics 2:43–50

    Article  PubMed  Google Scholar 

  • Carvalho CR, Gonçalves VN, Pereira CB, Johann S, Galliza IV, Alves TMA, Rabello A, Sobral MEG, Zani CL, Rosa CA, Rosa LH (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

    Article  Google Scholar 

  • Connell L, Staudigel H (2013) Fungal diversity in a dark oligotrophic volcanic ecosystem (DOVE) on Mount Erebus, Antarctica. Biology 2:798–809

    Article  PubMed Central  PubMed  Google Scholar 

  • Fell JW, Scorzetii G, Connel L, Graig S (2006) Biodiversity of micro-eukaryotes in Antarctic Dry Valley soils with <5% soil moisture. Soil Biol Biochem 38:3107–3119

    Article  CAS  Google Scholar 

  • Furbino LE, Godinho VM, Santiago IF, Pellizari FM, Alves TMA, Zani CL, Sales PAJ, Romanha AJ, Carvalho AGO, Gil LHVG, Rosa CA, Rosa LH (2014) Fungal communities associated with endemic macroalgae across the latitudinal gradient in Antarctica: occurrence, diversity and bioprospecting for antimicrobial, antiparasitic, and antiviral activities. Microb Ecol 67:775–787

    Article  PubMed  Google Scholar 

  • Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya N, Pupo D, Alves TMA, Sales 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gonçalves VN, Campos LS, Melo IS, Pellizari VH, Rosa CA, Rosa LH (2013) Penicillium solitum: a mesophilic, psychrotolerant fungus present in marine sediments from Antarctica. Polar Biol 36:1823–1831

    Article  Google Scholar 

  • Johann S, Rosa LH, Rosa CA, Perezc P, Cisalpino PS, Zani CL, Cota BB (2012) Antifungal activity of altenusin isolated from the endophytic fungus Alternaria sp. against the pathogenic fungus Paracoccidioides brasiliensis. Rev Iberoam Micol 29:205–209

    Article  PubMed  Google Scholar 

  • Khan A, Williams K, Nevalainen H (2003) Testing the nematophagous biological control strain Paecilomyces lilacinus 251 for paecilotoxin production. FEMS Microbiol Lett 227:107–111

    Article  CAS  PubMed  Google Scholar 

  • Khan Z, Ahmad S, Al-Ghimlas F, Al-Mutairi S, Joseph L, Chandy R, Sutton DA, Guarro J (2012) Purpureocillium lilacinum as a cause of cavitary pulmonary disease: a new clinical presentation and observations on atypical morphologic characteristics of the isolate. J Clin Microbiol 50:1800–1804

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CAB International, Wallingford

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Madariaga-Mazón A, González-Andrade M, González MC, Glenn AE, Cerda-García-Rojas CM, Mata R (2013) Absolute configuration of acremoxanthone C, a potent calmodulin inhibitor from Purpureocillium lilacinum. J Nat Prod 76:1454–1460

    Article  PubMed  Google Scholar 

  • Melo IS, Santos SN, Rosa LH, Parma MM, Silva LJ, Queiroz SCN, Pellizari VH (2013) Isolation and biological activities of an endophytic Mortierella alpina strain from the Antarctic moss Schistidium antarctici. Extremophiles 18:15–23

    Article  PubMed  Google Scholar 

  • Mercantini R, Marsella R, Cervellati MC (1989) Keratinophilic fungi isolated from Antarctic soil. Mycopathologia 106:47–52

    Article  CAS  PubMed  Google Scholar 

  • Mikami Y, Yazawa K, Fukushima K, Arai T, Udagawa S, Samson RA (1989) Paecilotoxin production in clinical or terrestrial isolates of Paecilomyces lilacinus strains. Mycopathologia 108:195–199

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Monks A, Scudiero D, Skehan P, Shoemaker R, Paull K, Vistica D, Hose C, Langley J, Parish CA, Cruz M, Smith SK, Zink D, Baxter J, Tucker-Samaras S, Collado J, Platas G, Bills G, Díez MT, Vicente F, Peláez F, Wilson K (1991) Antisense-guided isolation and structure elucidation of pannomycin, a substituted cis-decalin from Geomyces pannorum. J Nat Prod 72:59–62

    Google Scholar 

  • Romanha AJ, de Castro SL, Soeiro MNC, Lannes-Vieira J, Ribeiro I, Talvani A, Bourdin B, Blum B, Olivieri B, Zani C, Spadafora C, Chiari E, Chatelain E, Chaves G, Calzada JE, Bustamante JM, Freitas-Junior LH, Romero LI, Bahia MT, Lotrowska M, Soares M, Andrade SG, Armstrong T, Degrave W, de Andrade ZA (2010) In vitro and in vivo experimental models for drug screening and development for Chagas disease. Mem Inst Oswaldo Cruz 105:233–238

    Article  CAS  PubMed  Google Scholar 

  • Parish CA, de la Cruz M, Smith SK, Zink D, Baxter J, Tucker-Samaras S, Collado J, Platas G, Bills G, Díez MT, Vicente F, Peláez F, Wilson K (2009) Antisense-guided isolation and structure elucidation of pannomycin, a substituted cis-decalin from Geomyces pannorum. J Nat Prod 72:59–62

  • 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

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141

    Article  Google Scholar 

  • Santiago IF, Alves TMA, Rabello A, Sales-Júnior PA, Romanha AJ, Zani CL, Rosa CA, Rosa LH (2012) Leishmanicidal and antitumoral activities of endophytic fungi associated with the Antarctic angiosperms Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. Extremophiles 16:95–103

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Teixeira MC, Jesus SR, Sampaio RB, Pontes CL, Santos WL (2002) A simple and reproducible method to obtain large numbers of axenic amastigotes of different Leishmania species. Parasitol Res 88:963–968

    Article  PubMed  Google Scholar 

  • Teles APC, Takahashi JA (2012) Paecilomide, a new acetylcholinesterase inhibitor from Paecilomyces lilacinus. Microbiol Res 168:204–210

    Article  PubMed  Google Scholar 

  • Tosi S, Casado B, Gerdol R, Caretta G (2002) Fungi isolated from Antarctic mosses. Polar Biol 25:262–268

    Google Scholar 

  • 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

    Google Scholar 

  • Zucconi L, Selbmann L, Buzzini P, Turchetti B, Guglielmin M, Frisvad JC, Onofri S (2012) Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol 35:749–757

    Article  Google Scholar 

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Acknowledgments

We acknowledge the financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Processes PROANTAR 407230/2013-0, INCT Criosfera, Universal 471721/2013-1, 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. We thank the Brazilian Navy for the logistic support. Additionally, we thank the Dr. D.I. Shapiro-Ilan USDA-ARS, SAA for the manuscript review.

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Authors and Affiliations

  1. Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P. O. Box 486, Belo Horizonte, MG, CEP 31270-901, Brazil

    Vivian N. Gonçalves, Camila R. Carvalho, Susana Johann, Graziele Mendes, Carlos A. Rosa & Luiz H. Rosa

  2. René Rachou Research Center, FIOCRUZ-MG, Belo Horizonte, MG, Brazil

    Tânia M. A. Alves, Carlos L. Zani, Policarpo A. S. Junior, Silvane M. F. Murta & Alvaro J. Romanha

  3. Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis, SC, Brazil

    Alvaro J. Romanha

  4. USDA-ARS, Natural Products Utilization Research Unit, University, MS, 38677, USA

    Charles L. Cantrell

Authors
  1. Vivian N. Gonçalves
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  2. Camila R. Carvalho
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  3. Susana Johann
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  4. Graziele Mendes
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  5. Tânia M. A. Alves
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  6. Carlos L. Zani
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  7. Policarpo A. S. Junior
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  8. Silvane M. F. Murta
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  9. Alvaro J. Romanha
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  10. Charles L. Cantrell
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  11. Carlos A. Rosa
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  12. Luiz H. Rosa
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Correspondence to Luiz H. Rosa.

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Gonçalves, V.N., Carvalho, C.R., Johann, S. et al. Antibacterial, antifungal and antiprotozoal activities of fungal communities present in different substrates from Antarctica. Polar Biol 38, 1143–1152 (2015). https://doi.org/10.1007/s00300-015-1672-5

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  • DOI: https://doi.org/10.1007/s00300-015-1672-5

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