Diversity of sponge-associated fungi from a mangrove forest in Kemujan Island, Karimunjawa National Park, Indonesia




Abstract. Sibero MT, Pribadi R, Larasati SJH, Calabon MS, Sabdono A, Subagiyo S, Frederick EH. 2021. Diversity of sponge-associated fungi from a mangrove forest in Kemujan Island, Karimunjawa National Park, Indonesia. Biodiversitas 22: 5695-5605. Plenty of studies have reported interesting biological properties and bioactive compounds from sponge-associated fungi in Indonesia. However, only a few studies consider their biodiversity. Most of the studies collected the sponge from the coral reef ecosystem and barely reported from the mangrove ecosystem. This study aimed to discover the biodiversity of sponge-associated fungi from a mangrove ecosystem using a DNA barcoding approach. Five mangrove-associated sponges were collected from a tidal mangrove forest in Kemujan Island, Karimunjawa National Park, Indonesia. In total, we isolated 56 sponge-associated fungi, which consisted of seven genera in the phylum Ascomycota (77.78%), one genus in the phylum Basidiomycota (11.11%), and one genus in the phylum Mucoromycota (11.11%). Trichoderma (n: 15, 26.79%), Aspergillus (n: 13, 23.21%) and Fusarium (n: 12, 21.45%) were the top three dominant genera. In addition, based on the association of fungi to its sponge hosts, Aspergillus, Aureobasidium, Fusarium, and Trichoderma are sponge-generalists; Absidia and Pestalotiopsis are sponge-associates; while Lasiodiplodia, Montagnula, and Wallemia are sponge-specialist.


Abdel-Azeem AM, Abdel-Azeem MA, Darwish AG, Nafady NA, Ibrahim NA. 2019. Fusarium: Biodiversity, Ecological Significances, and Industrial Applications. In: Recent Advancement in White Biotechnology Through Fungi. Springer Nature, Switzerland. DOI: DOI: https://link.springer.com/chapter/10.1007/978-3-030-10480-1_6
Becking, LE, Cleary DFR, de Voogd NJ. 2013. Sponge Species Composition, Abundance, and Cover in Marine Lakes and Coastal Mangroves in Berau, Indonesia. Mar. Ecol. Prog. Ser. 481: 105–20. DOI: http://www.int-res.com/abstracts/meps/v481/p105-120/
Bell JJ, Jompa J, Haris A, Werorilangi S, Shaffer M, Mortimer C. 2018. Domination of mesophotic ecosystems in the Wakatobi Marine National Park (Indonesia) by sponges, soft corals and other non-hard coral species. J. Mar. Biolog. Assoc. U.K. 99(4): 771-775. DOI: https://doi.org/10.1017/S0025315418000917
Benoit I et al. 2013. Aspergillus: Genomics of a Cosmopolitan Fungus. In: Genomics of Soil- and Plant-Associated Fungi. Springer Nature, Switzerland. DOI: https://link.springer.com/chapter/10.1007/978-3-642-39339-6_5
Bovio E, Garzoli L, Poli A, Prigione V, Firsova D, McCormack GP, Varese GC. 2018. The Culturable mycobiota associated with three Atlantic sponges, including two new species: Thelebolus balaustiformis and T. spongiae. Fungal Syst. Evol. 1: 141–67. DOI: https://dx.doi.org/10.3114%2Ffuse.2018.01.07
Bovio E, Garzoli L, Poli A, Luganini A, Villa P, Musumeci R, McCormack GP, Cocuzza CE, Gribaudo G, Mehiri M, Varese GC. 2019. Marine fungi from the sponge Grantia compressa: biodiversity, chemodiversity, and biotechnological potential. Marine Drugs 17(4). DOI: https://dx.doi.org/10.3390%2Fmd17040220
Calabon MS, Sadaba RB, Campos WL. 2019. Fungal diversity of mangrove-associated sponges from New Washington, Aklan, Philippines. Mycology 10(1): 6–21. DOI: https://doi.org/10.1080/21501203.2018.1518934
Calcinai B, Bastari A, Makapedua DM, Cerrano C. 2017. Mangrove sponges from Bangka Island (North Sulawesi, Indonesia) with the description of a new species. J. Mar. Biolog. Assoc. U.K. 97(6): 1417–22. DOI: https://doi.org/10.1017/S0025315416000710
Chakraborty SK. 2019. Bioinvasion and Environmental Perturbation: Synergistic Impact on Coastal–Mangrove Ecosystems of West Bengal, India. In: Makowski C., Finkl C. (eds) Impacts of Invasive Species on Coastal Environments. Coastal Research Library, vol 29. Springer, Cham. https://doi.org/10.1007/978-3-319-91382-7_6
Chalearmsrimuang T, Ismail SI, Mazlan N, Suasaard S, Dethoup T. 2019. Marine-derived fungi: a promising source of halo tolerant biological control agents against plant pathogenic fungi. J. Pure. Appl. Microbio. 13(1): 209–23. DOI: https://dx.doi.org/10.22207/JPAM.13.1.22
Després VR, Huffman JA et al. 2012. Primary biological aerosol particles in the atmosphere: a review. Tellus B: Chem. Phys. Meteorol. 64(1). DOI: https://doi.org/10.3402/tellusb.v64i0.15598
Dissanayake AJ, Bhunjun CS, Maharachchikumbura SSN, Liu JK. 2020. Applied aspects of methods to infer phylogenetic relationships amongst fungi. Mycosphere 11(1): 2652-2676. DOI: https://www.mycosphere.org/pdf/MYCOSPHERE_11_1_18.pdf
Fang J, Han X, Xie L, Liu M, Qiao G, Jiang J, Zhuo R. 2014. Isolation of salt stress-related genes from Aspergillus glaucus CCHA by random overexpression in Escherichia coli. Sci. World J. DOI: https://doi.org/10.1155/2014/620959
Gel-Hemed I, Atanasova L, Komon-Zelazowska M, Druzhinina IS, Viterbo A, Yarden O. 2011. Marine isolates of Trichoderma spp. As potential halotolerant agents of biological control for arid-zone agriculture. Appl. Environ. Microbiol 77(15): 5100–5109. DOI: https://doi.org/10.1128/AEM.00541-11
González-Rivero M, Yakob L, Mumby PJ. 2011. The role of sponge competition on coral reef alternative steady states. Ecol. Modell. 222(11): 1847–53. DOI: https://doi.org/10.1016/j.ecolmodel.2011.03.020
Hapsari RW, Hartoko A, Hendrarto B. 2020. Mangrove vulnerability index and carbon algorithm using sentinel-2a satellite data at Kemujan Island, Karimunjawa Islands, Indonesia. AACL Bioflux 13(3): 1453–62.
Harris JL. 2000. Letter to the editor: safe, low-distortion tape touch method for fungal slide mounts. J. Clin. Microbiol. 38(12): 4683–84. DOI: https://doi.org/10.1128/jcm.38.12.4683-4684.2000
Hongsanan S, Hyde KD, Bahkali AH, Camporesi E, Chomnunti P, Ekanayaka H, Gomes AAM, Hofstetter V, Jones EBG, Pinho DB, Pereira OL, Tian Q, Wanasinghe DN, Xu JC, Buyck B.. 2015. Fungal biodiversity profiles 11-20. Cryptogamie, Mycologie 36(3): 355–80. DOI: https://doi.org/10.7872/crym/v36.iss3.2015.355
Imhoff JF. 2016. Natural products from marine fungi - still an underrepresented resource. Mar. Drugs 14(1). DOI: https://doi.org/10.3390/md14010019
Indraningrat AAG, Smidt H, Sipkema D. 2016. Bioprospecting sponge-associated microbes for antimicrobial compounds. Mar. Drugs 14(5). DOI: https://doi.org/10.3390/md14050087
Indrayanti E, Zainuri M et al. 2019. Larval dispersal model of coral acropora in the Karimunjawa Waters, Indonesia. Biodiversitas 20(7): 2068–75. DOI: https://doi.org/10.13057/biodiv/d200738
Ismet MS, Bengen DG et al. 2020. Associative-mesofauna abundance and its correlation with sponges antibacterial activity in seagrass ecosystem. The 4th EMBRIO International Symposium and the 7th International Symposium of East Asia Fisheries and Technologists Association. IPB University, Bogor, 5-6 August 2019. [Indonesian] DOI: 10.1088/1755-1315/404/1/012007
Johnson KVA, Burnet PWJ. 2016. Microbiome: should we diversify from diversity?. Gut Microbes 7(6): 455–58. DOI: https://doi.org/10.1080/19490976.2016.1241933
Jones EBG, Pang KL, Abdel-Wahab MA, Scholz B, Hyde KD, Boekhout T, Ebel R, Rateb ME, Henderson L, Sakayaroj J, Seutrong S, Dayarathne MC, Kumar V, Raghukumar S, Sridhar KR, Bahkali AHA, Gleason FH, Norphanphoun C. 2019. An online resource for marine fungi. Fungal Diversity 96: 347-433. DOI: https://doi.org/10.1007/s13225-019-00426-5
Jones EBG, Seutrong S, Sakayaroj J, Bahkali AH, Abdel-Wahab MA, Boekhout T, Pang K-L. 2015. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Diversity 73: 1-72. DOI: https://doi.org/10.1007/s13225-015-0339-4
Kamal M, Hartono H, Wicaksono P, Adi NS, Arjasakusuma S. 2016. Assessment of mangrove forest degradation through canopy fractional cover in Karimunjawa Island, Central Java, Indonesia. Geoplanning: J. Geomat. Plann. 3(2): 107-16. DOI: https://doi.org/10.14710/geoplanning.3.2.107-116
Kohlmeyer J, Kohlmeyer E. 1979. Marine Mycology: The Higher Fungi. Academic Press, New York. DOI: https://doi.org/10.1016/C2013-0-10998-1
Li Q, Wang G. 2009. Diversity of fungal isolates from three Hawaiian marine sponges. Microbiol. Res. 164(2): 233–41. DOI: https://doi.org/10.1016/j.micres.2007.07.002
Liu WC, Li CQ, Zhu P, Yang JL, Cheng KD. 2010. Phylogenetic diversity of culturable fungi associated with two marine sponges: Haliclona simulans and Gelliodes carnosa, collected from the Hainan Island coastal waters of the South China Sea. Fungal Diversity 42: 1–15. DOI: https://doi.org/10.1007/s13225-010-0022-8
Ludwig JA, Reynolds JF. 1988. Statistical Ecology: A Primer on Methods and Computing. John Wiley & Sons, Inc., New Jersey.
Maldonado M, Cortadellas N, Trillas MA, Rützler K. 2005. Endosymbiotic yeast maternally transmitted in a marine sponge. Biol. Bull. 209(2): 94–106. DOI: https://doi.org/10.2307/3593127
Mares MCD, Sipkema D, Huang S, Bunk B, Overmann J, van Elsas JD. 2017. Host specificity for bacterial, archaeal and fungal communities determined for high- and low-microbial abundance sponge species in two genera. Front. Microbiol. DOI: https://doi.org/10.3389/fmicb.2017.02560
Menezes CBA, Bonugli-Santos RC et al. 2010. Microbial diversity associated with algae, ascidians and sponges from the North Coast of São Paulo State, Brazil. Microbiol. Res. 165(6): 466–82. DOI: https://doi.org/10.1016/j.micres.2009.09.005
Nehren U, Wicaksono P. 2018. Mapping soil carbon stocks in an oceanic mangrove ecosystem in Karimunjawa Islands, Indonesia. Estuar. Coast. Shelf Sci. 214: 185–93. DOI: https://doi.org/10.1016/j.ecss.2018.09.022
Nguyen MTHD, Thomas T. 2018. Diversity, host-specificity and stability of sponge-associated fungal communities of co-occurring sponges. PeerJ 2018(6): 1–26. DOI: https://doi.org/10.7717/peerj.4965
Pang KL, Chiang MWL, Guo SY, Shih CY, Dahms HU, Hwang JS, Cha HJ. 2020. Growth study under combined effects of temperature, ph and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island hydrothermal vent field, Taiwan. PLoS ONE 15(5): 1–24. DOI: https://doi.org/10.1371/journal.pone.0233621
Pérez-Llano Y, Rodriguez-Pupo EC et al. 2020. Stress reshapes the physiological response of halophile fungi to salinity. Cells 9(3): 1–21. DOI: https://dx.doi.org/10.3390%2Fcells9030525
Pielou EC. 1966. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13(C): 131–44. DOI: https://doi.org/10.1016/0022-5193(66)90013-0
Pita L, Rix L, Slaby BM, Franke A, Hentschel U. 2018. The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6(1): 46. DOI: https://doi.org/10.1186/s40168-018-0428-1
Puryono S, Suryanti S. 2019. Degradation of mangrove ecosystem in Karimunjawa Island based on public perception and management. The 4th International Conference on Tropical and Coastal Region Eco Development. Universitas Diponegoro, Semarang, 30-31 October 2018. DOI: 10.1088/1755-1315/246/1/012080
Raghukumar S. 2017. Fungi in Coastal and Oceanic Marine Ecosystems: Marine Fungi Fungi in Coastal and Oceanic Marine Ecosystem. Marine Fungi. DOI: 10.1007/978-3-319-54304-8
Riddell RW, 1950. Permanent stained mycological preparationsobtained by slide culture. Mycologia 42: 265–270. DOI: https://doi.org/10.2307/3755439
Sabdaningsih A, Liu Y, Mettal U, Heep J, Riyanti, Wang L, Cristianawati O, Nuryadi H, Sibero MT, Marner M, Radjasa OK, Sabdono A, Trianto A, Schäberle TF. 2020. A new citrinin derivative from the Indonesian. Mar. Drugs 18(227). DOI: https://doi.org/10.3390/md18040227
Setiawan E, Muzaki FK, Ashuri NM. 2018. Shallow water sponges that associated to mangrove ecosystem at Labuhan conservation area in Sepulu, Bangkalan, Madura, East Java Province. NICHE J. Trop. Biol. 1(2): 19-29.
Setiawan E, Muzaki FK, Nurhayati APD, Maulidina N. 2019. Record of shallow-water sponges in Simeulue Island, Aceh Province, Indonesia. Biodiversitas 20(11): 3246–57. DOI: https://doi.org/10.13057/biodiv/d201117
Sibero MT, Radjasa OK, Sabdono A, Trianto A, Triningsih DW, Hutagaol ID. 2018. Antibacterial activity of Indonesian sponge associated fungi against clinical pathogenic multidrug resistant bacteria. J. Appl. Pharm. Sci. 8(2): 088–094. DOI: 10.7324/JAPS.2018.8214
Sibero MT, Igarashi Y, Radjasa OK, Sabdono A, Trianto A, Zilda DS, Wijaya YJ. 2019. Sponge-associated fungi from a mangrove habitat in Indonesia?: species composition, antimicrobial activity, enzyme screening and bioactive profiling. Int. Aquatic Res. 11(2): 173–86. DOI: https://doi.org/10.1007/s40071-019-0227-8
Sibero MT, Zhou T, Fukaya K, Urabe D, Radjasa OKK, Sabdono A, Trianto A, Igarashi Y.. 2019. Two new aromatic polyketides from a sponge-derived Fusarium. Beilstein J. Org. Chem. 15: 2941–47. DOI: https://doi.org/10.3762/bjoc.15.289
Sibero MT, Zhou T et al. 2020. Chromanone-type compounds from marine sponge-derived Daldinia eschscholtzii KJMT FP 4.1. J. Appl. Pharm. Sci. 10(1): 1–7. DOI: 10.7324/JAPS.2020.101001
Smith B, Wilson JB. 1996. A consumer’s guide to evenness indices. Oikos 76: 70–82. DOI: https://doi.org/10.2307/3545749
Tennakoon DS, Hyde KD, Wanasinghe DN, Bahkali AH, Camporesi E, Khan S, Phookamsak R. 2016. Taxonomy and phylogenetic appraisal of Montagnula jonesii sp. Nov. (Didymosphaeriaceae, Pleosporales). Mycosphere 7(9): 1346–56. DOI: 10.5943/mycosphere/7/9/8
Vahidi F, Fatemi SMR, Danehkar A, Mashinchian A, Nadushan RM. 2020. Benthic macrofaunal dispersion within different mangrove habitats in Hara Biosphere Reserve, Persian Gulf. Int. J. Environ. Sci. Technol. 17(3): 1295–1306. https://doi.org/10.1007/s13762-019-02469-2
Winata A, Yuliana E, Hewindati YT, Djatmiko WA. 2020. Assessment of mangrove carrying capacity for ecotourism in Kemujan Island , Karimunjawa National Park , Indonesia. AES Biofux 12(1): 83–97.
Yang Q, Zhang W, Franco CMM. 2019. Symbiotic microbiomes of coral reefs sponges and corals Response of Sponge Microbiomes to Environmental Variations. Springer, Netherlands. DOI: 10.1007/978-94-024-1612-1

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