Abstract
Seagrasses are flowering plants inhabiting coastal and marine environments, with a worldwide distribution. They serve as feeding, breeding and nursery grounds for economically important marine organisms including endangered species. The tropical seagrass Enhalus acoroides was collected from Had Khanom-Mu Ko Thale Tai National Park, southern Thailand. The objectives of this study were to investigate for the presence of endophyte assemblages in E. acoroides, as well as to describe the diversity of endophytes based on LSU, ITS1, 2, 5.8S rDNA sequence analyses. Forty-two fungal assemblages were isolated and identified through molecular data. This resulted in a diversity of fungal groups of Ascomycota (98%) and Basidiomycota (2%). Three major Ascomycota classes including the Sordariomycetes (36%), Eurotiomycetes (33%) and Dothideomycetes (24%) were determined. The predominant ascomycete orders were the Hypocreales, followed by the Eurotiales and the Capnodiales, respectively. Additionally one taxon belonged to the Russulales, Basidiomycota and was possibly mycorrhiza. This study confirms that E. acoroides harbors a wide diversity of fungal endophytes, and provides a baseline for further studies on fungal-host plant interactions.
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Abdel-Wahab MA, El-Sharouny HM (2002) Ecology of subtropical mangrove fungi with emphasis on Kandelia candel mycota. In: Fungi in Marine Environment (ed. K.D. Hyde). Fungal Divers Res Ser 7:247–265
Ajello L, McGinnis MR, Camper J (2004) An outbreak of phaeohyphomycosis in rainbow trout caused by Scolecobasidium humicola. Mycopathologia 62:15–22
Alker AP, Smith GW, Kim K (2001) Characterization of Aspergillus sydowii (Thom & Church), a funagal pathogen of Carribbean sea fan corals. Hydrobiologia 460:105–111
Alva P, Mckenzire EHC, Pointing SP, Pena-Murala R, Hyde KD (2002) Do seagrasses habour endophytes? In: Fungi in Marine Environments (ed. K.D. Hyde). Fungal Divers Res Ser 7:167–178
Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biology Review 21:51–66
Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206
Câmara MPS, Ramaley AW, Castlebury LA, Palm ME (2003) Neophaeosphaeria and Phaeosphaeriopsis, segregates of Paraphaeosphaeria. Mycol Res 107:516–522
Câmera MPS, Palm ME, van Berkum P, Stewart EL (2001) Systematics of Paraphaeosphaeria: a molecular and morphological approach. Mycol Res 105:41–56
Cantrell SA, Casillas-Martínez L, Molina M (2006) Characterization of fungi from hypersaline environments of solar salterns using morphological and molecular techniques. Mycol Res 110:962–970
Caroll GC (1995) Forest endophytes: pattern and process. Can J Bot 73 (suppl.):S1316–S1324
Clay K (1991) Endophytes as antagonists of plant pests. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer-Verlag, New York, pp 331–357
Crous PW, Schubert K, Braun U, de Hoog GS, Hocking AD, Shin H-D, Groenewald JZ (2007) Opportunistic, human-pathogenic species in the Herpotrichiellaceae are phenotypically similar to saprobic or phytopathogenic species in the Venturiaceae. Stud Mycol 58:185–217
Cuomo V, Vanzanella F, Fresi E, Mazzella L, Scipione MB (1982) Micoflora delle fenerogame dell ‘Isolad’ Ischia: Posidonia oceanica (L.) Delile Cymodocea nodosa (Ucria) Aschers. Bulletin Musea Institute Biologia, Universiti Genova 50:162–166
Cuomo V, Vanzanella F, Fresi F, Cinelli F, Mazzella L (1985) Fungal flora of Posidonia oceanica and its ecological significance. Trans Br Mycol Soc 84:35–40
Cuomo, V., Vanzanella, F., D’Antonio, S., Mazzella, L. and Bula, M.C. (1989). Micoflora della fanerogama marina Zostera noltii Hornem. dell’isola d’ischia. Oebalia XV-I: 129–136.
Curlevski NJA, Chambers SM, Anderson IC, Cairney JWG (2009) Identical genotypes of an ericoid mycorrhiza-forming fungus occur in roots of Epacris pulchella (Ericaceae) and Leptospermum polygalifolium (Myrtaceae) in an Australian sclerophyll forest. FEMS Microbiol Ecol 67:411–420
Devarajan PT, Suryanarayanan TS, Geetha V (2002) Endophytic fungi associated with the tropical seagrass Halophila ovalis (Hydrocharitaceae). Indian J Mar Sci 31:73–74
Duong LM, Jeewon R, Lumyong S, Hyde KD (2006) DGGE coupled with ribosomal DNA phylogenies reveal uncharacterized fungal phylotypes on living leaves of Magnolia liliifera. Fungal Divers 23:121–138
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327
Guo LD, Hyde KD, Liew ECD (2001) Detection and taxonomic placement of endophytic fungi within frond tissues of Livistona chinensis based on rDNA sequences. Mol Phylogenet Evol 20:1–13
Hall T (2004) BioEdit 6.0.7. Department of microbiology, North Carolina State University. (http://www.mbio.ncsu.edu/BioEdit/bioedit.html)
Higgins KL, Arnold AE, Miadlikowska J, Sarvate SD, Lutzoni F (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555
Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33:61–75
Huang WY, Cai YZ, Surveswaran S, Hyde KD, Corke H, Sun M (2009) Molecular phylogenetic identification of endophytic fungi isolated from three Artemisia species. Fungal Divers 36:69–88
Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics17: 754–755. (http://morphbank.ebc.uu.se/mrbayes/downloadphp)
Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173
Hyde KD, Jones EBG, Leano L, Pointing SB, Poonyth AD, Vrijmoed LLP (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1161
Jensen PR, Jenkins KM, Porter D, Fenical W (1998) Evidence that a new antibiotic flavone glycoside chemically defends the sea grass Thalassia testudinum against zoosporic fungi. Appl Environ Microbiol 64:1490–1496
Jones EBG, Hyde KD (2004) Introduction to Thai fungal diversity. In: Jones EBG, Tanticharoen M, Hyde KD (eds) Thai fungal diversity. BIOTEC, Thailand, pp 7–35
Jones EBG, Pilantanapak A, Chatmala I, Sakayaroj J, Phongpaichit S, Choeyklin R (2006) Thai marine fungal diversity. Songklanakarin Science and Technology Journal 28:687–715
Jones EBG, Sakayaroj J, Suetrong S, Somrithipol S, Pang KL (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:1–203
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth and Bisby’s dictionary of the fungi, 9th edn. CABI, London
Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order of Hominoidea. J Mol Evol 29:170–179
Koh LL, Tan TK, Chou LM, Goh NKC (2002) Antifungal properties of Singapore gorgonians: a preliminary study. J Exp Mar Biol Ecol 273:121–130
Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic, New York
Kumaresan V, Suryanarayanan TS (2001) Occurrence and distribution of endophytic fungi in a mangrove community. Mycol Res 105:1388–1391
Kumaresan V, Suryanarayanan TS, Johnson JA (2002) Ecology of mangrove endophytes. In: Fungi in Marine Environments (ed. K.D. Hyde). Fungal Divers Res Ser 7:145–166
Kuo J (1984) Structural aspects of apoplast fungal hyphae in a marine angiosperm, Zostera muelleri Irmisch ex Aschers. (Zosteraceae). Protoplama 121:1–7
Kuo J, Ridge RW, Lewis SV (1990) The leaf internal morphology and ultrastructure of Zostera muelleri Irmisch ex Aschers. (Zosteraceae): a comparative study of the intertidal and subtidal forms. Aquat Bot 36:217–236
Landvik S (1996) Neolecta, a fruit-body-producing genus of the basal ascomycetes, as shown by SSU and LSU rDNA sequences. Mycol Res 100:199–202
Leano EM, Vrijmoed LLP, Jones EBG (1998) Physiological studies on Halophytophthora vesicula (Straminipilous fungi) isolated from fallen mangrove leaves from Mai Po, Hong Kong. Bot Mar 41:411–419
Li Q, Wang G (2009) Diversity of fungal isolates from three Hawaiian marine sponges. Microbiol Res 164:233–241
Li WC, Zhou J, Guo SY, Guo LD (2007) Endophytic fungi associated with lichens in Baihua mountain of Beijing, China. Fungal Divers 25:69–80
Lodge DJ, Fisher PJ, Sutton BC (1996) Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia 88:733–738
Logan A (1992) Seagrass beds. In: Thomas MLH, Logan A (eds) A guide to the ecology of shoreline and shallow water marine communities of Bermuda. Brown, Dubuque, pp 69–92 Bermuda Biological Station for Research Special Publication #30
Mitchell AM, Strobel GA, Hess WM, Vargas PN, Ezra D (2008) Muscodor crispans, a novel endophyte from Ananas ananassoides in the Bolivian Amazon. Fungal Divers 31:37–43
Morrison-Gardiner S (2002) Dominant fungi from Australian coral reefs. Fungal Divers 9:105–121
Newell SY, Fell JW (1980) Mycoflora of turtlegrass (Thalassia testudinum Konig) as recorded after seawater incubation. Bot Mar 23:265–275
Nielsen J, Nielsen PH, Frisvad JC (1999) Fungal depside, guisinol, from a marine derived strain of Emericella unguis. Phytochemistry 50:263–265
Nilsson RH, Ryberg M, Abarenkoy K, Sjökvist E, Kristiansson E (2009) The ITS region as a target for characterization of fungal communities using emergent sequencing technologies. FEMS Microbiol Lett 296:97–101
O'Donnell K, Cigelnik E, Weber NS, Trappe JM (1997) Phylogenetic relationships among ascomycetous truffles and the true and false morels inferred from 18S and 28S ribosomal DNA sequence analysis. Mycologia 89:48–65
Ohori A, Endo S, Sano A, Yokoyama K, Yamaguchi M, Kamei K, Miyaji M, Nishimura K (2006) Rapid identification of Ochroconis gallopava by a loop-mediated isothermal amplification (LAMP) method. Vet Microbiol 114:359–365
Okane I, Nakagiri A, Ito I (2001) Assemblages of endophytic fungi on Bruguiera gymnorrhiza in the Shira River Basin, Iriomote Is. Inst Ferment Res Comm-Osaka 20:41–49
Oses R, Valenzuela S, Freer J, Sanfuentes E, Rodríguez J (2008) Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Diversity 33:77–86
Pang KL, Vrijmoed LLP, Goh TK, Plaingam N, Jones EBG (2008) Fungal endophytes associated with Kandelia candel (Rhizophoraceae) in Mai Po Nature Reserve, Hong Kong. Bot Mar 51:171–178
Petrini O, Stone J, Carroll FE (1982) Endophytic fungi in evergreen shrubs in western Oregon: a preliminary study. Can J Bot 60:789–796
Phang S-M (2000) Seagrasses of Malaysia. University of Malaya, Malaysia
Phongpaichit S, Preedanan S, Rungjindamai N, Sakayaroj J, Benzies C, Chuaypat J, Plathong, S (2006) Aspergillosis of the gorgonian sea fan Annella sp., after the 2004 tsunami at Mu Ko Similan National Park, Andaman Sea, Thailand. Coral Reefs (Short communication). doi 10.1007/s00338-006-0104-y
Preedanon S (2007) Screening and identification of sea fan-derived fungi that produce antimicrobial substances. Prince of Songkla University, Thailand M.Sc Thesis
Raghukumar C (2008) Marine fungal biotechnology: an ecological perspective. Fungal Divers 31:19–35
Rodríguez GM (2008) Potential of fungal endophytes from Thalassia testudinum Bank ex K.D. Koenig as producers of bioactive compounds. University of Puerto Rico, Puerto Rico M.Sc. Thesis
Ross C, Puglisi MP, Paul VJ (2008) Antifungal defenses of seagrasses from the Indian River Lagoon, Florida. Aquat Bot 88:134–141
Rungjindamai N (2005) Endophytic fungi from Garcinia spp. which produce antimicrobial substances. Prince of Songkla University, Thailand M.Sc. Thesis
Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones EBG (2008) Molecular characterization of basidiomycetous endophytes isolated from leaves, rachis and petioles of the oil palm, Elaeis guineensis, in Thailand. Fungal Divers 33:139–161
Saikkonen K, Wäli P, Helander M, Faeth SH (2004a) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280
Saikkonen K, Helander M, Faeth SH (2004b) Fungal endophytes: hitchhikers of the green world. In: Gillings M, Holmes A (eds) Plant microbiology. BIOS, Oxford, pp 77–95
Sánchez Márquez S, Bills GF, Zabalgogeazcoa I (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fungal Divers 33:87–100
Schulz B, Boyle C (2005) The endophyte continuum. Mycol Res 109:661–686
Seena S, Wynberg N, Bärlocher F (2008) Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Divers 30:1–14
Siegel MR, Schardl CL (1991) Fungal endophytes of grasses: detrimental and beneficial association. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer-Verlag, New York, pp 198–221
Slim FJ, Hemmings MA, Cocheretde la Moriniere E, van der Velde G (1996) Tidal exchange of macrolitter between a mangrove forest and adjacent seagrass beds (Gazi Bay, Kenya). Neth J Aquat Ecol 30:119–128
Smith GW, Komchi AM, Hayasaka SS (1982) Heavy metal sensitivity of seagrass rhizoplane and sediment bacteria. Bot Mar 25:19–24
Suryanarayanan TS, Kumaresan V (2000) Endophytic fungi of some halophytes from an estuarine mangrove forest. Mycol Res 104:1465–1467
Suryanarayanan TS, Johnson JA (2005) Fungal endophytes of tropical plants: a critical review. In: Suryanarayanan T, Johri BN (eds) Microbial diversity: current perspectives and potential applications. I.K. International, New Delhi, pp 207–224
Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer, Sunderland
Tao G, Liu ZY, Hyde KD, Lui XZ, Yu ZN (2008) Whole rDNA analysis reveals novel and endophytic fungi in Bletilla ochracea (Orchidaceae). Fungal Divers 33:101–122
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Trisuwan K, Rukachaisirikul V, Sukpondma Y, Preedanon S, Phongpaichit S, Rungjindamai N, Sakayaroj J (2008) Epoxydons and a pyrone from the marine-derived fungus Nigrospora sp. PSU-F5. J Nat Prod 71:1323–1326
Trisuwan K, Rukachaisirikul V, Sukpondma Y, Preedanon S, Phongpaichit S, Sakayaroj J (2009) Pyrone derivatives from the marine-derived fungus Nigrospora sp. PSU-F18. Phytochemistry. doi:10.1016/j.phytochem.2009.01.008
Tsukiboshi T, Chung WH, Yoshida S (2005) Cochliobolus heveicola sp. nov. (Bipolaris heveae) causes brown stripe of Bermuda grass and Zoysia grass. Mycoscience 46:17–21
Vergeer LHT, Develi A (1997) Phenolic acids in healthy and infected leaves of Zostera marina and their growth-limiting properties towards Labyrithula zosterae. Aquat Bot 58:65–72
Vergeer LHT, Aarts TL, de Groot JD (1995) The “wasting disease” and the effect of abiotic factors (light intensity, temperature, salinity) and infection with Labyrinthula zosterae on the phenolic content of Zostera marina shoots. Aquat Bot 52:35–44
Wang G, Li Q, Zhu P (2008) Phylogenetic diversity of culturable fungi associated with the Hawaiian Sponges Suberites zeteki and Gelliodes fibrosa. Antonie Van Leeuwenhoek 93:163–174
Wang Y, Guo LD, Hyde KD (2005) Taxonomic placement of sterile morphotypes of endophytic fungi from Pinus tabulaeformis (Pinaceae) in notheast China based on rDNA sequences. Fungal Divers 20:235–260
White TF, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA gene for phylogenetics. In: Innis MA, Gelfand DH, Sninsky FS, White TT (eds) PCR protocol: a guide to methods and applications. Academic, San Diego, pp 315–322
Wilson WL (1998) Isolation of endophytes from seagrasses from Bermuda. The University of New Brunswick, Canada M.Sc. Thesis
Wilson D (2000) Ecology of woody plant endophytes. In: Bacon CW, Whites JF (eds) Microbial endophytes. Dekker, USA, pp 389–420
Zalar P, de Hoog GS, Schroers H-J, Crous PW, Groenewalf JZ, Gunde-Cimernam N (2007) Phylogeny and ecology of the ubiquitous saprobe Cladosporium sphaerospermum, with descriptions of seven new species from hypersaline environments. Stud Mycol 58:157–183
Zuccaro A, Mitchell JI (2005) Fungal communities of seaweeds. In: Dighton J, White JF Jr, Oudemans P (eds) The fungal community. CRC, New York, pp 533–579
Zuccaro A, Schulz B, Mitchell JI (2003) Molecular detection of ascomycetes associated with Fucus serratus. Mycol Res 107:1451–1466
Zuccaro A, Summerfield RC, Gams W, Schroers H-F, Mitchell JI (2004) A new Acremonium species associated with Fucus spp., and its affinity with a phylogentically distinct marine Emericellopsis clade. Stud Mycol 50:283–297
Zuccaro A, Schoch CL, Spatafora JW, Kohlmeyer J, Draeger S, Mitchell JI (2008) Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl Environ Microbiol 74:931–941
Acknowledgements
This work was supported by the TOTAL Corporate Foundation, TOTAL E&P Thailand and the TRF/BIOTEC Special Program for Biodiversity Research and Training Grant BRT R_351004. We acknowledge Prof. Morakot Tanticharoen, Dr. Kanyawim Kirtikara and Dr. Lily Eurwilaichitr for continued support. Special thanks go to Ms. Satinee Suetrong, Mr. Anupong Klaysuban and Mr. Nattawut Rungjindamai for field assistance.
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Sakayaroj, J., Preedanon, S., Supaphon, O. et al. Phylogenetic diversity of endophyte assemblages associated with the tropical seagrass Enhalus acoroides in Thailand. Fungal Diversity 42, 27–45 (2010). https://doi.org/10.1007/s13225-009-0013-9
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DOI: https://doi.org/10.1007/s13225-009-0013-9