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Biatriospora (Ascomycota: Pleosporales) is an ecologically diverse genus including facultative marine fungi and endophytes with biotechnological potential

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Abstract

Biatriospora (Ascomycota: Pleosporales, Biatriosporaceae) is a genus with unexplored diversity and poorly known ecology. This work expands the Biatriospora taxonomic and ecological concept by describing four new species found as endophytes of woody plants in temperate forests of the Czech Republic and in tropical regions, including Amazonia. Ribosomal DNA sequences, together with protein-coding genes (RPB2, EF1α), growth rates and morphology, were used for species delimitation and description. Ecological data gathered by this and previous studies and the inclusion of sequences deposited in public databases show that Biatriospora contains species that are endophytes of angiosperms in temperate and tropical regions as well as species that live in marine or estuarine environments. These findings show that this genus is more diverse and has more host associations than has been described previously. The possible adaptations enabling the broad ecological range of these fungi are discussed. Due to the importance that Biatriospora species have in bioprospecting natural products, we suggest that the species introduced here warrant further investigation.

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References

  • Ahmed S, Van De Sande W, Stevens D, Fahal A, van Diepeningen A, Menken S, de Hoog G (2014) Revision of agents of black-grain eumycetoma in the order Pleosporales. Persoonia 33:141–154. doi:10.3767/003158514X684744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahuja M, Chiang Y-M, Chang S-L, Praseuth MB, Entwistle R, Sanchez JF, Lo H-C, Yeh H-H, Oakley BR, Wang CCC (2012) Illuminating the diversity of aromatic polyketide synthases in Aspergillus nidulans. J Amer Chem Soc 134:8212–8221. doi:10.1021/ja3016395

    Article  CAS  Google Scholar 

  • Angelini P, Rubini A, Gigante D, Reale L, Pagiotti R, Venanzoni R (2012) The endophytic fungal communities associated with the leaves and roots of the common reed Phragmites australis in Lake Trasimeno (Perugia, Italy) in declining and healthy stands. Fungal Ecol 5:683–693

    Article  Google Scholar 

  • Arnold AE, Engelbrecht BMJ (2007) Fungal endophytes double minimum leaf conductance in seedlings of a tropical tree. J Trop Ecol 23:369–372. doi:10.1016/j.funeco.2012.03.001

    Article  Google Scholar 

  • Bolaños J, León LF, Ochoa E, Darias J, Raja HA, Shearer CA, Miller AN, Vanderheyden P, Porras-Alfaro A, Caballero-George C (2015) Phylogenetic diversity of sponge-associated fungi from the Caribbean and the Pacific of Panama and their in vitro effect on angiotensin and endothelin receptors. Mar Biotechnol 17:533–564. doi:10.1007/s10126-015-9634-z

    Article  PubMed  Google Scholar 

  • Borelli D (1976) Pyrenochaeta mackinnonii nova species agente de micetoma. Castellania 4:227–234

    Google Scholar 

  • Bugni TS, Ireland CM (2004) Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat Prod Rep 21:143–163. doi:10.1039/b301926h

    Article  CAS  PubMed  Google Scholar 

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556. doi:10.2307/3761358

    Article  CAS  Google Scholar 

  • Chagas FO, Caraballo-Rodriguez AM, Pupo MT (2015) Endophytic fungi as a source of novel metabolites. In: Zeilinger S, Martin J-F, Garcia-Estrada C (eds) Biosynthesis and molecular genetics of fungal secondary metabolites, vol 2. Springer, New York, pp 123–176. doi:10.1007/978-1-4939-2531-5_8

    Chapter  Google Scholar 

  • Chinnaraj S (1993) Higher marine fungi from mangroves of Andaman and Nicobar Islands. Sydowia 45:109–115

    Google Scholar 

  • Damare S, Singh P, Raghukumar S (2012) Biotechnology of marine fungi. In: Raghukumar C (ed) Biology of marine fungi. Springer, Heidelberg, pp 277–297. doi:10.1007/978-3-642-23342-5_14

    Chapter  Google Scholar 

  • de Gruyter J, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous PW (2013) Redisposition of phoma-like anamorphs in Pleosporales. Stud Mycol 75:1–36. doi:10.3114/sim0004

    Article  PubMed  Google Scholar 

  • de Hoog GS, Zalar P, Van Den Ende BG, Gunde-Cimerman N (2005) Relation of halotolerance to human-pathogenicity in the fungal tree of live: an overview of ecology and evolution under stress. In: Gunde-Cimerman N, Oren A, Plemenitas A (eds) Adaptations to life at high salt concentrations in Archaea, Bacteria and Eukarya. Springer, New York, pp 185–200. doi:10.1007/1-4020-3633-7

    Google Scholar 

  • Debbab A, Aly A, Proksch P (2012) Endophytes and associated marine derived fungi-ecological and chemical perspectives. Fungal Diversity 57:45–83. doi:10.1007/s13225-012-0191-8

    Article  Google Scholar 

  • Dreyfuss MM, Chapela IH (1994) Potential of fungi in the discovery of novel, low-molecular weight pharmaceuticals. In: Gullo VP (ed) Discovery of novel natural products with therapeutic potential. Newnes, Boston, pp 49–80

    Chapter  Google Scholar 

  • Gardes M, Bruns D (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Molec Ecol 2:113–118. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  Google Scholar 

  • Gazis R, Chaverri P (2015) Wild trees in the Amazon basin harbor a great diversity of beneficial endosymbiotic fungi: Is this evidence of protective mutualism? Fungal Ecol 17:18–29. doi:10.1016/j.funeco.2015.04.001

    Article  Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environm Microbiol 61:1323–1330

    CAS  Google Scholar 

  • Gu W (2009) Bioactive metabolites from Alternaria brassicicola ML-P08, an endophytic fungus residing in Malus halliana. World J Microbiol Biotechnol 25:1677–1683. doi:10.1007/s11274-009-0062-y

    Article  CAS  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  • Hansen FT, Gardiner DM, Lysøe E, Fuertes PR, Tudzynski B, Wiemann P, Sondergaard TE, Giese H, Brodersen DE, Sørensen JL (2015) An update to polyketide synthase and non-ribosomal synthetase genes and nomenclature in Fusarium. Fungal Genet Biol 75:20–29. doi:10.1016/j.fgb.2014.12.004

    Article  CAS  PubMed  Google Scholar 

  • Haugen P, Simon DM, Bhattacharya D (2005) The natural history of group I introns. Trends Genet 21:111–119. doi:10.1016/j.tig.2004.12.007

    Article  CAS  PubMed  Google Scholar 

  • Heimberger J, Cade HC, Padgett J, Sittaramane V, Shaikh A (2015) Total synthesis of Herbarin A and B, determination of their antioxidant properties and toxicity in zebrafish embryo model. Bioorg Med Chem Lett 25:1192–1195. doi:10.1016/j.bmcl.2015.01.065

    Article  CAS  PubMed  Google Scholar 

  • Higginbotham SJ, Arnold AE, Ibañez A, Spadafora C, Coley PD, Kursar TA (2013) Bioactivity of fungal endophytes as a function of endophyte taxonomy and the taxonomy and distribution of their host plants. PLoS ONE 8:e73192. doi:10.1371/journal.pone.0073192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyde KD, Borse B (1986) Marine fungi from Seychelles: 5 Biatriospora marina gen. and sp. nov. from mangrove wood. Mycotaxon 26:263–270

    Google Scholar 

  • Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Diversity 33:163–173. doi:10.1371/journal.pone.0141444

    Google Scholar 

  • Hyde KD, Jones EBG, Liu J-K, Ariyawansa H, Boehm E, Boonmee S, Braun U, Chomnunti P, Crous PW, Dai D-Q, Diederich P, Dissanayake A, Doilom M, Doveri F, Hongsanan S, Jayawardena R, Lawrey JD, Li Y-M, Liu Y-X, Lucking R, Monkai J, Muggia L, Nelsen MP, Pang K-L, Phookamsak R, Senanayake IC, Shearer CA, Suetrong S, Tanaka K, Thambugala KM, Wijayawardene NN, Wikee S, Wu H-X, Zhang Y, Aguirre-Hudson B, Alias SA, Aptroot A, Bahkali AH, Bezerra JL, Bhat DJ, Camporesi E, Chukeatirote E, Gueidan C, Hawksworth DL, Hirayama K, De Hoog S, Kang J-C, Knudsen K, Li W-J, Li X-H, Liu Z-Y, Mapook A, McKenzie EHC, Miller AN, Mortimer PE, Phillips AJL, Raja HA, Scheuer C, Schumm F, Taylor JE, Tian Q, Tibpromma S, Wanasinghe DN, Wang Y, Xu J-C, Yacharoen S, Yan J-Y, Zhang M (2013) Families of Dothideomycetes. Fungal Diversity 63:1–313. doi:10.1007/s13225-013-0263-4

    Article  Google Scholar 

  • Jones EBG, Pilantanapak A, Chatmala I, Sakayaroj J, Phongpaichit S, Choeyklin R (2006) Thai marine fungal diversity. Songklanakarin J Sci Technol 28:687–708

    Google Scholar 

  • Jones EBG, Sakayaroj J, Suetrong S, Somrithipol S, Pang KL (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Diversity 35:1–187

    Google Scholar 

  • Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. In: Posada D (ed) Bioinformatics for DNA sequence analysis, vol 537. Methods in molecular biology. Humana Press Inc, Totowa, pp 39–64. doi:10.1007/978-1-59745-251-9_3

    Chapter  Google Scholar 

  • Kelly KL, Judd DB (1976) Color: universal language and dictionary of names, vol 440. US Department of Commerce, National Bureau of Standards, Washington

    Book  Google Scholar 

  • Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ (2015) Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Crit Rev Biotechnol 35:62–74. doi:10.3109/07388551.2013.800018

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Mizuno T, Nakajima H, Hamasaki T (1992) Altechromones A and B, new plant growth regulators produced by the fungus, Alternaria sp. Biosci Biotechnol Biochem 56:1664–1665. doi:10.1271/bbb.56.1664

    Article  CAS  Google Scholar 

  • Kjer J, Debbab A, Aly AH, Proksch P (2010) Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nature Protoc 5:479–490. doi:10.1038/nprot.2009.233

    Article  CAS  Google Scholar 

  • Kohlmeyer J (1981) Distribution and ecology of conidial fungi in marine habitats. In: Cole GT, Kendrick B (eds) Biology of conidial fungi. Academic Press, New York, NY, pp 357–372

    Chapter  Google Scholar 

  • Kohlmeyer J, Volkmann-Kohlmeyer B (2003) Fungi from coral reefs: a commentary. Mycol Res 107:386–387. doi:10.1017/S0953756203227775

    Article  PubMed  Google Scholar 

  • Kolařík M, Jankowiak R (2013) Vector affinity and diversity of Geosmithia fungi living on subcortical insects inhabiting Pinaceae species in Central and Northeastern Europe. Microbial Ecol 66:682–700. doi:10.1007/s00248-013-0228-x

    Article  Google Scholar 

  • Koukol O, Kelnarová I, Černý K (2015) Recent observations of sooty bark disease of sycamore maple in Prague (Czech Republic) and the phylogenetic placement of Cryptostroma corticale. Forest Pathol 45:21–27. doi:10.1111/efp.12129

    Article  Google Scholar 

  • Kowalski T, Kraj W, Bednarz B (2016) Fungi on stems and twigs in initial and advanced stages of dieback of European ash (Fraxinus excelsior) in Poland. Eur J Forest Res 135:565–579. doi:10.1007/s10342-016-0955-x

    Article  Google Scholar 

  • Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798. doi:10.1016/j.chembiol.2012.06.004

    Article  CAS  PubMed  Google Scholar 

  • Kushner DJ (1978) Life in high salt and solute concentrations. In: Kushner DJ (ed) Microbial life in extreme environments. Academic, New York, pp 317–386

    Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Molec Biol Evol 16:1799–1808

    Article  CAS  PubMed  Google Scholar 

  • Liu J-K, Phookamsak R, Dai D-Q, Tanaka K, Jones EBG, Xu J-C, Chukeatirote E, Hyde KD (2014) Roussoellaceae, a new pleosporalean family to accommodate the genera Neoroussoella gen. nov., Roussoella and Roussoellopsis. Phytotaxa 181:1–33. doi:10.11646/phytotaxa.181.1.1

    Article  Google Scholar 

  • Navarri M, Jégou C, Meslet-Cladière L, Brillet B, Barbier G, Burgaud G, Fleury Y (2016) Deep subseafloor fungi as an untapped reservoir of amphipathic antimicrobial compounds. Mar Drugs 14:50. doi:10.3390/md14030050

    Article  PubMed Central  Google Scholar 

  • Nikoh N, Fukatsu T (2001) Evolutionary dynamics of multiple group I introns in nuclear ribosomal RNA genes of endoparasitic fungi of the genus Cordyceps. Molec Biol Evol 18:1631–1642

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233

    Google Scholar 

  • O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molec Phylogen Evol 7:103–116. doi:10.1006/mpev.1996.0376

    Article  Google Scholar 

  • Opatz T, Kolshorn H, Thines E, Anke H (2008) Ascomycones A-C, heptaketide metabolites from an unidentified ascomycete. J Nat Prod (Lloydia) 71:1973–1976. doi:10.1021/np800570w

    Article  CAS  Google Scholar 

  • Panno L, Bruno M, Voyron S, Anastasi A, Gnavi G, Miserere L, Varese GC (2013) Diversity, ecological role and potential biotechnological applications of marine fungi associated to the seagrass Posidonia oceanica. New Biotechnol 30:685–694. doi:10.1016/j.nbt.2013.01.010

    Article  CAS  Google Scholar 

  • Passarini MR, Santos C, Lima N, Berlinck RG, Sette LD (2013) Filamentous fungi from the Atlantic marine sponge Dragmacidon reticulatum. Arch Microbiol 195:99–111. doi:10.1007/s00203-012-0854-6

    Article  CAS  PubMed  Google Scholar 

  • Paz Z, Komon-Zelazowska M, Druzhinina IS, Aveskamp MM, Shnaiderman A, Aluma Y, Carmeli S, Ilan M, Yarden O (2010) Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge. Fungal Diversity 42:17–26. doi:10.1007/s13225-010-0020-x

    Article  Google Scholar 

  • Pažoutová S, Šrůtka P, Holuša J, Chudíčková M, Kolařík M (2010) Diversity of xylariaceous symbionts in Xiphydria woodwasps: role of vector and a host tree. Fungal Ecol 3:392–401. doi:10.1371/journal.pone.0143566

    Article  Google Scholar 

  • Pažoutová S, Šrůtka P, Holuša J, Chudíčková M, Kubátová A, Kolařík M (2012) Liberomyces gen. nov. with two new species of endophytic coelomycetes from broadleaf trees. Mycologia 104:198–210. doi:10.3852/11-081

    Article  PubMed  Google Scholar 

  • Ramírez-Camejo LA, Zuluaga-Montero A, Lázaro-Escudero M, Hernández-Kendall V, Bayman P (2012) Phylogeography of the cosmopolitan fungus Aspergillus flavus: is everything everywhere? Fungal Biol 116:452–463. doi:10.1016/j.funbio.2012.01.006

    Article  PubMed  Google Scholar 

  • Rateb ME, Ebel R (2011) Secondary metabolites of fungi from marine habitats. Nat Prod Rep 28:290–344. doi:10.1039/C0NP00061B

    Article  CAS  PubMed  Google Scholar 

  • Ravindran C, Naveenan T, Varatharajan GR, Rajasabapathy R, Meena RM (2012a) Antioxidants in mangrove plants and endophytic fungal associations. Bot Mar 55:269–279. doi:10.1515/bot-2011-0095

    Article  CAS  Google Scholar 

  • Ravindran C, Varatharajan GR, Rajasabapathy R, Vijayakanth S, Kumar AH, Meena RM (2012b) A role for antioxidants in acclimation of marine derived pathogenic fungus (NIOCC 1) to salt stress. Microbial Pathog 53:168–179. doi:10.1016/j.micpath.2012.07.004

    Article  CAS  Google Scholar 

  • Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98. doi:10.3852/mycologia.97.1.84

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez R, White Jr J, Arnold AE, Redman R (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330. doi:10.1111/j.1469-8137.2009.02773.x

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Rundell SM, Spakowicz DJ, Narváez-Trujillo A, Strobel SA (2015) The biological diversity and production of volatile organic compounds by stem-inhabiting endophytic fungi of Ecuador. J Fungi 1:384–396. doi:10.3390/jof1030384

    Article  Google Scholar 

  • Rypien KL, Andras JP, Harvell C (2008) Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii. Molec Ecol 17:4068–4078. doi:10.1111/j.1365-294X.2008.03894.x

    Article  Google Scholar 

  • Sakayaroj J, Preedanon S, Phongpaichit S, Buatong J, Chaowalit P, Rukachaisirikul V (2012) Diversity of endophytic and marine-derived fungi associated with marine plants and animals. In: Jones EBG, Pang K-L (eds) Marine fungi and fungal-like organisms. Marine and freshwater botany. de Gruyter, Berlin, pp 291–328. doi:10.1515/9783110264067.291

    Google Scholar 

  • Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI (2004) Occurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol Lett 239:319–323. doi:10.1016/j.femsle.2004.09.005

    Article  CAS  PubMed  Google Scholar 

  • Schuffler A, Liermann JC, Kolshorn H, Opatz T, Anke H (2009) New naphthoquinone derivatives from the Ascomycete IBWF79B-90A. Z Naturf C 64:25–31. doi:10.1515/znc-2009-1-205

    Google Scholar 

  • Schulz B, Boyle C, Draeger S, Römmert A-K, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004. doi:10.1017/S0953756202006342

    Article  CAS  Google Scholar 

  • Shaw JJ, Spakowicz DJ, Dalal RS, Davis JH, Lehr NA, Dunican BF, Orellana EA, Narváez-Trujillo A, Strobel SA (2015) Biosynthesis and genomic analysis of medium-chain hydrocarbon production by the endophytic fungal isolate Nigrograna mackinnonii E5202H. Appl Microbiol Biotechnol 99:3715–3728. doi:10.1007/s00253-014-6206-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shushni MAM (2009) Isolation, structure elucidation and pharmacological investigation of bioactive secondary metabolites from in vitro cultivated marine fungi. Ph.D. Dissertation, Ernst Moritz Arndt University, Greifswald, Germany

  • Shushni MAM, Mentel R, Lindequist U, Jansen R (2009) Balticols A-F, new naphthalenone derivatives with antiviral activity, from an ascomycetous fungus. Chem Biodivers 6:127–137. doi:10.1002/cbdv.200800150

    Article  CAS  PubMed  Google Scholar 

  • Shushni MA, Singh R, Mentel R, Lindequist U (2011) Balticolid: a new 12-membered macrolide with antiviral activity from an ascomycetous fungus of marine origin. Mar Drugs 9:844–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shushni MAM, Azam F, Lindequist U (2013) Oxasetin from Lophiostoma sp. of the Baltic Sea: identification, in silico binding mode prediction and antibacterial evaluation against fish pathogenic bacteria. Nat Prod Commun 8:1223–1226. doi:10.2147/DDDT.S67778

    CAS  PubMed  Google Scholar 

  • Smith SA, Tank DC, Boulanger L-A, Bascom-Slack CA, Eisenman K, Kingery D, Babbs B, Fenn K, Greene JS, Hann BD, Keehner J, Kelley-Swift EG, Kembaiyan V, Lee SJ, Li P, Light DY, Lin EH, Ma C, Moore E, Schorn MA, Vekhter D, Nunez PV, Strobel GA, Donoghue MJ, Strobel SA (2008) Bioactive endophytes warrant intensified exploration and conservation. PLoS ONE 3:e3052. doi:10.1371/journal.pone.0003052

    Article  PubMed  PubMed Central  Google Scholar 

  • Spakowicz DJ, Strobel SA (2015) Biosynthesis of hydrocarbons and volatile organic compounds by fungi: bioengineering potential. Appl Microbiol Biotechnol 99:4943–4951. doi:10.1007/s00253-015-6641-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stodůlková E, Man P, Kuzma M, Černý J, Císařová I, Kubátová A, Chudíčková M, Kolařík M, Flieger M (2015) A highly diverse spectrum of naphthoquinone derivatives produced by the endophytic fungus Biatriospora sp. CCF 4378. Folia Microbiol 60:259–267. doi:10.1007/s12223-014-0366-7

    Article  Google Scholar 

  • Suetrong S, Schoch CL, Spatafora JW, Kohlmeyer J, Volkmann-Kohlmeyer B, Sakayaroj J, Phongpaichit S, Tanaka K, Hirayama K, Jones EBG (2009) Molecular systematics of the marine Dothideomycetes. Stud Mycol 64:155–173. doi:10.3114/sim.2009.64.09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Supaphon P, Phongpaichit S, Rukachaisirikul V, Sakayaroj J (2014) Diversity and antimicrobial activity of endophytic fungi isolated from the seagrass Enhalus acoroides. Indian J Geo-Mar Sci 43:785–797. doi:10.1371/journal.pone.0072520

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molec Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tresner HD, Hayes JA (1971) Sodium chloride tolerance of terrestrial fungi. Appl Microbiol 22:210–213

    CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. A Guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

  • Xing X, Guo S (2011) Fungal endophyte communities in four Rhizophoraceae mangrove species on the south coast of China. Ecol Res 26:403–409. doi:10.1007/s11284-010-0795-y

    Article  Google Scholar 

  • Xu W, Luo Z-H, Guo S, Pang K-L (2016) Fungal community analysis in the deep-sea sediments of the Pacific Ocean assessed by comparison of ITS, 18S and 28S ribosomal DNA regions. Deep-Sea Res 1. Oceanogr Res Pap 109:51–60. doi:10.1016/j.dsr.2016.01.001

    Article  CAS  Google Scholar 

  • Zak JC, Wildman HG (2004) Fungi in stressful environments. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi, inventory and monitoring methods. Elsevier/Academic, London, pp 303–315

    Chapter  Google Scholar 

  • Zhang X-y, G-l Tang, Xu X-y, Nong X-h, Qi S-H (2014) Insights into deep-sea sediment fungal communities from the East Indian Ocean using targeted environmental sequencing combined with traditional cultivation. PLoS ONE 9:e109118. doi:10.1371/journal.pone.0109118

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank K. Prášil (Dept. of Botany, Charles University) for help with collecting and isolating of B. antibiotica. The endophytes isolated from Ecuador were obtained with a collecting and research permit provided to SAS by the Ministerio del Ambiente of Ecuador, and the ones collected in Peru were obtained under the collecting permit 0035-2011-AG-DJFFS-DGEFFS provided to RG by the Ministerio de Agricultura of Peru. The authors would like to thank Percy Vargas Nunez for his help with collection and identification of the Ecuadorian host plants and Durga Thakral, Shan Kuang, Samantha Lee and Rahul Dalal for isolating the Ecuadorian endophytes used in this study. This work was supported by the Czech Science Foundation Project No. 13-16565S, LD-COST CZ project LD13039, COST action FA1103: Endophytes in Biotechnology and Agriculture, and BIOCEV (CZ.1.05/1.1.00/02.0109)—Biotechnology and Biomedicine Centre of the Academy of Sciences and Charles University from the European Regional Development Fund. IK was supported by the project GAUK 420214. DJS was supported by the NIH T15 LM007056-29. Fungi associated with Hevea and Virola were collected under a project funded by NSF grants DEB-925672 and DEB-1019972 to P. Chaverri (University of Maryland, USA).

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Authors and Affiliations

  1. Institute of Microbiology of the CAS, v.v.i., Vídeňská 1083, 142 20, Prague 4, Czech Republic

    Miroslav Kolařík, Alena Nováková & Milada Chudíčková

  2. Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, 06511, USA

    Daniel J. Spakowicz, Jeffrey Shaw, Giovanni C. Forcina, Ki Woong Kang & Scott A. Strobel

  3. Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN, 37996, USA

    Romina Gazis

  4. Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, 128 01, Praha 2, Czech Republic

    Alena Kubátová & Ivana Kelnarová

  5. Department of Plant Science and Landscape Architecture, University of Maryland, 2112 Plant Sciences Building, College Park, MD, 20742, USA

    Demetra Skaltsas

  6. Laboratorio de Biotecnología Vegetal, Pontificia Universidad Católica del Ecuador, 17 01 21 84, Quito, Ecuador

    Carolina E. Portero & Alexandra Narváez-Trujillo

Authors
  1. Miroslav Kolařík
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  2. Daniel J. Spakowicz
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  3. Romina Gazis
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  4. Jeffrey Shaw
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  5. Alena Kubátová
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  6. Alena Nováková
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  7. Milada Chudíčková
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  8. Giovanni C. Forcina
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  9. Ki Woong Kang
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  10. Ivana Kelnarová
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  11. Demetra Skaltsas
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  12. Carolina E. Portero
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  13. Scott A. Strobel
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  14. Alexandra Narváez-Trujillo
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Corresponding author

Correspondence to Miroslav Kolařík.

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The authors declare that they have no conflict of interest.

Additional information

Handling editor: S. W. Peterson.

Electronic supplementary material

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Information on Electronic supplementary material

Online Resource 1. Growth response to increasing NaCl concentration and growth on sea water agar in five isolates of Biatriospora.

Online Resource 2. List of ITS rDNA sequences used in phylogenetic comparisons (Fig. 2). Source of origin, geographical location and data about secondary metabolite production is provided.

Online Resource 3. Growth of Biatriospora spp. on three different media.

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Kolařík, M., Spakowicz, D.J., Gazis, R. et al. Biatriospora (Ascomycota: Pleosporales) is an ecologically diverse genus including facultative marine fungi and endophytes with biotechnological potential. Plant Syst Evol 303, 35–50 (2017). https://doi.org/10.1007/s00606-016-1350-2

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  • DOI: https://doi.org/10.1007/s00606-016-1350-2

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