Abstract
Fungi occur in mangroves as saprobes, pathogens, and endophytes of a wide range of timber host substrates and may also be isolated from the water column and bottom sediments. In this study, we explore their biodiversity within a single mangrove forest at Muthupet, Tamil Nadu, India. The study showed a rich diversity of fungi on five decaying host substrates (out of seven host substrates) collected in the intertidal zone, resulting in 78 marine fungal taxa in 67 genera from 11 field collections and 6215 samples. Of the 78 taxa, 56 species (in 47 genera) belong to the Ascomycota and two species (2 genera) to Basidiomycota with the remaining 20 species representing asexual fungi (18 genera). Some fungal species were repeatedly reported: Verruculina enalia (21.65%) was the most frequently collected fungus; Marinosphaera mangrovei (9.2%), Rimora mangrovei (9.15%), Okeanomyces cucullatus (8.7%), Halocryptosphaeria bathurstensis (6%) in the frequent category, Paraconiothyrium cyclothyroides (4.5%), Hysterium rhizophorae (3.5%), Sclerococcum haliotrephum (3.6%), Lulworthia sp. (3.6%), and Farasanispora avicenniae (3%) were infrequently collected. Of the host substrates, Avicennia marina wood pieces harbored 49 fungal species of which 19 were unique. Two-way ANOVA revealed that fungal species richness was not affected irrespective of the collection season (P = 0.239) but was significantly dependent on the wood species (P < 0.001).
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Abdel-wahab MA, Hodhod MS, Bahkali AHA, Jones EBG (2014) Marine fungi of Saudi Arabia. Bot Mar 57:323–335. https://doi.org/10.1515/bot-2014-0010
Abdel-Wahab MA, Dayarathne MC et al (2017) New saprobic marine fungi and a new combination. Bot Mar 60:469–488. https://doi.org/10.1007/s13225-019-00426-5
Alias SA, Kuthubutheen AJ, Jones EBG (1995) Frequency of occurrence of fungi on wood in Malaysian mangroves. Hydrobiologia 295:97–106
Alias SA, Zainuddin N, Jones EBG (2010) Biodiversity of marine fungi in Malaysian mangroves. Bot Mar 53:545–554. https://doi.org/10.1515/BOT.2010.066
Barata M (2002) Fungi on the halophyte Spartina maritima in salt marshes. Fungi Mar Environ 179–193
Binder M, Hibbett DS, Molitoris HP (2001) Phylogenetic relationships of the marine gasteromycete Nia vibrissa. Mycologia 93:679–688. https://doi.org/10.1080/00275514.2001.12063199
Binder M, Hibbett DS, Wang Z, Farnham WF (2006) Evolutionary relationships of Mycaureola dilseae (Agaricales), a basidiomycete pathogen of a subtidal rhodophyte. Am J Bot 93:547–556. https://doi.org/10.3732/ajb.93.4.547
Blum LK, Roberts MS, Garland JL, Mills AL (2004) Distribution of microbial communities associated with the dominant high marsh plants and sediments of the United States east coast. Microb Ecol 48:375–388
Borse BD, and Hyde KD (1989) Marine fungi from India. III. Acrocordiopsis patilii gen. et. sp. nov. from mangrove wood. Mycotaxon
Borse BD, Borse KN, Pawar NS, Tuwar AR (2013) Marine fungi from India-XII. A revised check list. IJMS 42:110–119
Borse BD, Pawar NS, Patil SY et al (2018) Aquatic fungi of India: fresh water and marine. BIOINFOLET-A Q J Life Sci 15:137–148
Chinnaraj S (1993) Higher marine fungi from mangroves of Andaman and Nicobar Islands. Sydowia 45:109–115
Chinnaraj S, Untawale AG (1992) Manglicolous fungi from India. Indian J Geo-Marine Sci 25:25–29
Cooke RC, Rayner ADM (1984) Ecology of saprophytic fungi. London: Longman
Cuomo V, Vanzanella F, Fresi E et al (1982) Micoflora delle fenerogame dellIsola d’Ischia: Posidonia oceanica (L.) Delile Cymodocea nodosa (Ucria) Aschers. Bull Mus Inst Biol Univ Genova 50:162–166
Cuomo V, Vanzanella F, Fresi E et al (1985) Fungal flora of Posidonia oceanica and its ecological significance. Trans Br Mycol Soc 84:35–40
Dayarathne MC, Jones EBG, Maharachchikumbura SSN et al (2020a) Morpho-molecular characterization of microfungi associated with marine based habitats. Mycosphere 11:1–188. https://doi.org/10.5943/mycosphere/11/1/1
Dayarathne MC, Wanasinghe DN, Devadatha B et al (2020b) Modern taxonomic approaches to identifying diatrypaceous fungi from marine habitats, with a novel genus Halocryptovalsa Dayarathne & KD Hyde, gen. nov. Cryptogam Mycol 41:21–67. https://doi.org/10.5252/cryptogamie-mycologie2020v41a3
Devadatha B, Sarma V (2018) Pontoporeia mangrovei sp. nov, a new marine fungus from an Indian mangrove along with a new geographical and host record of Falciformispora lignatilis. Curr Res Environ Appl Mycol 8:238–246. https://doi.org/10.5943/cream/8/2/8
Devadatha B, Sarma VV, Wanasinghe DN et al (2017) Introducing the new Indian mangrove species, Vaginatispora microarmatispora (Lophiostomataceae) based on morphology and multigene phylogenetic analysis. Phytotaxa 329:139–149. https://doi.org/10.11646/phytotaxa.329.2.4
Devadatha B, Sarma VV, Jeewon R et al (2018a) Thyridariella, a novel marine fungal genus from India: morphological characterization and phylogeny inferred from multigene DNA sequence analyses. Mycol Prog 17:1–14. https://doi.org/10.1007/s11557-018-1387-4
Devadatha B, Sarma VV, Jeewon R, Jones EBG (2018b) Morosphaeria muthupetensis sp. nov.(Morosphaeriaceae) from India: morphological characterization and multigene phylogenetic inference. Bot Mar 61:395–405. https://doi.org/10.1515/bot-2017-0124
Devadatha B, Sarma VV, Ariyawansa HA, Jones EBG (2018c) Deniquelata vittalii sp. nov., a novel Indian saprobic marine fungus on Suaeda monoica and two new records of marine fungi from Muthupet mangroves East Coast of India. Mycosphere 9:565–582. https://doi.org/10.5943/mycosphere/9/3/8
Devadatha B, Mehta N, Baghela A, Sarma VV (2019) Vittaliana mangrovei gen. et sp. nov. in Phaeosphaeriaceae from Pondicherry mangroves in India, based on morphology and multigene phylogeny. Cryptogamie Mycologie 40:117–132. https://doi.org/10.5252/cryptogamiemycologie2019v40a7
Devadatha B, Jones EBG, Pang KL, Abdel-Wahab MA, Hyde KD, Sakayaroj J, Bahkali AH, Calabon M, Sarma VV, Sutreong S Zhang S (2021) Occurrence and geographical distribution of mangrove fungi. Fungal Divers 106:137–227. https://doi.org/10.1007/s13225-020-00468-0
Ellis MB (1971) Dematiaceous hyphomycetes. Kew: Commonwealth Mycological Institute
Ellis MB (1976) More dematiaceous hyphomycetes. Kew: Commonwealth Mycological Institute, 507
Fell JW, Hunter IL (1979) Fungi associated with the decomposition of the black rush, Juncus roemerianus, in south Florida. Mycologia 322–342
Gordon RA, Sutton DA, Thompson EH et al (2012) Cutaneous phaeohyphomycosis caused by Paraconiothyrium cyclothyrioides. J Clin Microbiol 50(11):3795–3798. https://doi.org/10.1128/JCM.01943-12
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9
Hongsanan S, Hyde KD, Phookamsak R et al (2020) Refined families of dothideomycetes: Dothideomycetidae and pleosporomycetidae. Mycosphere 11:1553–2107. https://doi.org/10.5943/mycosphere/11/1/13
Hyde KD, Jones EBG (1988) Marine mangrove fungi. Mar Ecol 9:15–33
Hyde KD, Jones EBG (1989) Ecological observations on marine fungi from the Seychelles. Bot J Linn Soc 100:237–254
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
Hyde KD, Alias SA (1999) Linocarpon angustatum sp. nov., and Neolinocarpon nypicola sp. nov. from petioles of Nypa fruticans, and a list of fungi from aerial parts of this host. Mycoscience 40:145–149. https://doi.org/10.1007/BF02464293
Hyde KD, Sarma VV (2000) Pictorial key to higher marine fungi. Mar Mycol a Pract approach Fungal Divers Press Hong Kong 86
Hyde KD, Jones EBG, Leaño E et al (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1161
Hyde KD, Norphanphoun C, Abreu VP et al (2017) Fungal diversity notes 603–708: taxonomic and phylogenetic notes on genera and species. Fungal Divers 87:1–235. https://doi.org/10.1007/s13225-017-0391-3
Hyde KD, Chaiwan N, Norphanphoun C, Boonmee S et al (2018) Mycosphere notes 169–224. Mycosphere 9:271–430. https://doi.org/10.5943/mycosphere/9/2/8
Hyde KD, de Silva NI, Jeewon R et al (2020a) AJOM new records and collections of fungi: 1–100. Asian J Mycol 3:22–294. https://doi.org/10.5943/ajom/3/1/3
Hyde KD, Dong Y, Phookamsak R et al (2020b) Fungal diversity notes 1151–1276: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers 100:5–277. https://doi.org/10.1007/s13225-020-00439-5
Jayasiri SC, Hyde KD, Ariyawansa HA et al (2015) The faces of fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Divers 74:3–18
Jones EBG (1982) Decomposition by basidiomycetes in aquatic environments. In: Symposium series-British Mycological Society
Jones EBG (2011) Are there more marine fungi to be described? Bot Mar 54:343–354. https://doi.org/10.1515/bot.2011.043
Jones EBG, Abdel-Wahab MA (2005) Marine fungi from the Bahamas Islands. Bot Mar 48:356–364. https://doi.org/10.1515/BOT.2005.048
Jones EBG, Read SJ, Moss ST et al (1996) Tirisporella gen. nov., an ascomycete from the mangrove palm Nypa fruticans. Can J Bot 74:1487–1495. https://doi.org/10.1139/b96-179
Jones EBG, Sakayaroj J, Suetrong S et al (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:187
Jones EBG, Pang K-L, Abdel-Wahab MA et al (2019) An online resource for marine fungi. Fungal Divers 96:347–433. https://doi.org/10.1007/s13225-019-00426-5
Jones EBG, Devadatha B, Abdel-Wahab MA et al (2020) Phylogeny of new marine Dothideomycetes and Sordariomycetes from mangroves and deep-sea sediments. Bot Mar 63:155–181. https://doi.org/10.1515/bot-2019-0014
Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. Southward, AJ, Tyler, PA, Young, CM Fuiman, LA (eds), New York: Adv Mar Biol Acad Press, 40:84–251. https://doi.org/10.1016/S0065-2881(01)40003-4
Kathiresan K, Rajendran N (2005) Mangrove ecosystems of the Indian Ocean region. IJMS 34:104–113
Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. New York: Acad Press. https://doi.org/10.1016/C2013-0-10998-1
Kohlmeyer J, Volkmann-Kohlmeyer B (1987) Marine fungi from Belize with a description of two new genera of ascomycetes. Bot Mar 30:195–204. https://doi.org/10.1515/botm.1987.30.3.195
Kohlmeyer J, Volkmann-Kohlmeyer B (1991) Illustrated key to the filamentous higher marine fungi. Bot Mar 34:1–61. https://doi.org/10.1515/botm.1991.34.1.1
Kohlmeyer J, Volkmann-Kohlmeyer B (2002) Fungi on Juncus and Spartina: new marine species of Anthostomella, with a list of marine fungi known on Spartina. Mycol Res 106:365–374. https://doi.org/10.1017/S0953756201005469
Kondo M, Goto H, Yamanaka K (2018) Case of Scedosporium aurantiacum infection detected in a subcutaneous abscess. Med Mycol Case Rep 20:26–27. https://doi.org/10.1016/j.mmcr.2018.01.003
Lex A, Gehlenborg N, Strobelt H et al (2014) UpSet: visualization of intersecting sets. IEEE Trans vis Comput Graph 20:1983–1992
Loilong A, Sakayaroj J, Rungjindamai N, et al (2012) 15 Biodiversity of fungi on the palm Nypa fruticans. Mar Fungi Fungal-like Org 273. https://doi.org/10.1515/9783110264067
Maria GL, Sridhar KR (2002) Richness and diversity of filamentous fungi on woody litter of mangroves along the west coast of India. Curr Sci 1573–1580
Maria GL, Sridhar KR (2003) Diversity of filamentous fungi on woody litter of five mangrove plant species from the southwest coast of India. Fungal Divers 14:109–126
Maria GL, Sridhar KR (2004) Fungal colonization of immersed wood in mangroves of the southwest coast of India. Can J Bot 82:1409–1418. https://doi.org/10.1139/b04-090
Naskar K, Mandal R (1999) Ecology and biodiversity of Indian mangroves. Daya Books
Natural Earth, Natural Earth Geo Features. Natural earth large scale 1:10 m data of river+lakes centerlines V 2.0, 2012. [Online]. http://www.naturalearthdata.com/downloads/10m-physical-vectors/10m-rivers-lake-centerlines/
Newell SY, Porter D (2002) Microbial secondary production from salt marsh-grass shoots, and its known and potential fates. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Springer, pp 159–185. https://doi.org/10.1007/0-306-47534-0_9
Patil SD, Borse BD (1983) Marine fungi from Maharashtra (India) III. Some fungi from mangroves. Indian Bot Reports 2:56–58
Patil SD, Borse BD (1985) Marine fungi from Indian mangroves. The mangroves proceedings on the national symposium on the biological utilization and conservation of Mangroves. Shivaji University Publication, Kolhapur, pp 151–152
Phookamsak R, Hyde KD, Jeewon R, et al (2019) Fungal diversity notes 929–1035: taxonomic and phylogenetic contributions on genera and species of fungi. Fungal Divers 1–273. https://doi.org/10.1007/s13225-019-00421-w
Pointing SB (1999) Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. Fungal Divers 2:17–33
Poon MOK, Hyde KD (1998) Biodiversity of intertidal estuarine fungi on Phragmites at Mai Po marshes, Hong Kong. Bot Mar 41:141–156. https://doi.org/10.1515/botm.1998.41.1-6.141
Poonyth AD, Hyde KD, Peerally A (1999) Intertidal fungi in Mauritian mangroves. Offpr Bot Mar 42:243–252. https://doi.org/10.1515/BOT.1999.028
QGIS Development Team (2016) QGIS geographic information system (version 3.12.1). Software. https://www.qgis.org
Raveendran K, Manimohan P (2007) Marine fungi of Kerala: a preliminary floristic and ecological study. Malabar Natural History Society. https://doi.org/10.13140/2.1.3699.8084
Ravikumar DR, Vittal BPR (1996) Fungal diversity on decomposing biomass of mangrove plant Rhizophora in Pichavaram estuary, east coast of India. IJMS 25:142–144
Sainty GR, Hosking J, Carr G, Adam P (2012) Estuary plants and what’s happening to them in south-east Australia. Sainty Books
Sarma VV (2016) Diversity of mangrove fungi on Rhizophora wood in Puducherry, Southeast coast of India. KAVAKA 46:37–39
Sarma VV, Hyde KD (2001) A review on frequently occurring fungi in mangroves. Fungal Divers 8:1–34
Sarma VV, Raghukumar S (2013) Manglicolous fungi from Chorao mangroves, Goa, West coast of India: diversity and frequency of occurrence. Nov Hedwigia 97:533–542
Sarma VV, Vittal BPR (2000) Biodiversity of mangrove fungi on different substrata of Rhizophora apiculata and Avicennia spp. from Godavari and Krishna deltas, east coast of India. Fungal Divers 5:23–41
Sarma VV, Vittal BPR (2001a) Biodiversity of manglicolous fungi on selected plants in the Godavari and Krishna deltas, east coast of India. Fungal Divers 6:115–130
Sarma VV, Devadatha B (2020) Fungal diversity in mangroves of India and a note on their medicinal potential. In: Patra JK, Mishra RR, Thatoi H (eds) Biotechnological utilization of mangrove resources. Elsevier, pp 153–224. https://doi.org/10.1016/B978-0-12-819532-1.00007-X
Sarma VV, Hyde KD, Vittal BPR (2001) Frequency of occurrence of mangrove fungi from the east coast of India. Hydrobiologia 455:41–53. https://doi.org/10.1023/A:1011983200976
Schmit JP, Shearer CA (2003) A checklist of mangrove-associated fungi, their geographical distribution and known host plants. Mycotaxon 85:423–477
Seifert K, Jones MG, Gams W, Kendrick B (2011) The genera of hyphomycetes. CBS Biodiversity series no. 9:1–997. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423
Shearer CA, Descals E, Kohlmeyer B et al (2007) Fungal biodiversity in aquatic habitats. Biodivers Conserv 16:49–67. https://doi.org/10.1007/s10531-006-9120-z
Simpson EH (1949) Measurement of diversity. Nature 163:688
Singh AK, Ansari A, Kumar D, Sarkar UK (2012) Status, biodiversity and distribution of mangroves in India: an overview. Uttar Pradhesh Sate Biodivers Board Mar Biodivers One Ocean Many Worlds Life 59–67
Sridhar KR (2009) Fungal diversity of Pichavaram mangroves, southeast coast of India. Nat Sci 7:1545–1740
Sridhar KR, Maria GL (2006) Fungal diversity on mangrove woody litter Rhizophora mucronata (Rhizophoraceae). Indian J Geo-Marine Sci 35:318–325
Sridhar KR, Alias SA, Pang K-L (2012) Mangrove fungi. In: Jones EBG, Pang KL. Marine fungi and fungal-like organisms. de Gruyter, Berlin, Germany, 2012. pp 253–271. https://doi.org/10.1515/9783110264067
Suetrong S, Schoch CL, Spatafora JW et al (2009) Molecular systematics of the marine Dothideomycetes. Stud Mycol 64:155–173. https://doi.org/10.3114/sim.2009.64.09
Suetrong S, Preedanon S, Klaysuban A et al (2017) Distribution and occurrence of manglicolous marine fungi from eastern and southern Thailand. Bot Mar 60:503–514. https://doi.org/10.1515/bot-2016-0107
Sutton BC (1980) The Coelomycetes. Fungi imperfecti with pycnidia, acervuli and stromata. Kew: Commonwealth Mycological Institute, 1–696 pp
Tan TK, Leong WF, Jones EBG (1989) Succession of fungi on wood of Avicennia alba and A. lanata in Singapore. Can J Bot 67:2686–2691. https://doi.org/10.1139/b89-346
Torzilli AP, Sikaroodi M, Chalkley D, Gillevet PM (2006) A comparison of fungal communities from four salt marsh plants using automated ribosomal intergenic spacer analysis (ARISA). Mycologia 98:690–698. https://doi.org/10.1080/15572536.2006.11832641
Van Ryckegem G, Verbeken A (2005) Fungal diversity and community structure on Phragmites australis (Poaceae) along a salinity gradient in the Scheldt estuary (Belgium). Nov Hedwigia 80:173–197
Vittal BPR, Sarma VV (2006) Diversity and ecology of fungi on mangroves of Bay of Bengal region - an overview. Indian J Mar Sci 35(4):308–317
Wong MKM, Hyde KD (2002) Fungal saprobes on standing grasses and sedges in a subtropic aquatic habitat. Fungal Divers Res Ser 7:195–212
Acknowledgements
V.V. Sarma would like to thank the Ministry of Earth Sciences (MOES), Govt. of India (MOES/36/OOIS/Extra/40/2014/PC-IV) for funding this work. He also would like to thank the Tamil Nadu Forest Department and District Forest Office, Tiruvarur, Tamil Nadu, for providing permission to collect samples. Department of Biotechnology, Pondicherry University, is thanked for providing the facilities. B. Devadatha would like to thank the Ministry of Earth Sciences, Govt. of India, for providing a fellowship. VVS thanks UGC-SAP and DST-FIST programs of Govt. of India for partial infrastructural support. E. B. Gareth Jones was supported under the Distinguished Scientist Fellowship Program (DSFP), King Saud University, Kingdom of Saudi Arabia. We thank the anonymous reviewers for their comments and suggestions which have improved the manuscript.
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This research was funded by the Ministry of Earth Sciences (MOES), Govt. of India, grant number (MOES/36/OO1S/Extra/40/2014/PC-IV).
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BD contributed in the investigation of the research work, methodology, formal analysis, software, data curation, writing the original draft of the manuscript, review, editing, and visualization. SG contributed in the statistical analyses, software, formal analysis, writing-review, editing type face, and data curation. EBG has contributed in review and editing of the manuscript, visualization and validation. VVS contributed in conceptualization, methodology, resources, supervision, project administration, funding acquisition, and review and editing of the manuscript. All authors reviewed and approved the manuscript.
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Bandarupalli, D., Jones, E.B.G., Ghate, S.D. et al. Biodiversity of marine fungi in mangroves with reference to Muthupet mangroves, Tamil Nadu, east coast of India. Mar. Biodivers. 51, 88 (2021). https://doi.org/10.1007/s12526-021-01214-8
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DOI: https://doi.org/10.1007/s12526-021-01214-8