The effect of culture media on the number and bioactivity of marine invertebrates associated fungi
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Abstract. Trianto A, Radjasa OK, Sibero MT, Sabdono A, Haryanti D, Zilullah WOM, Syanindyta AR, Bahry MS, Widiananto PA, Helmi M, Armono HD, Supriadi, Igarashi Y. 2020. The effect of culture media on the number and bioactivity of marine invertebrates associated fungi. Biodiversitas 21: 407-412. Marine ecosystem is rich with microorganisms such as bacteria and fungi either as free-living or in association with macro-organisms. Marine invertebrates provide suitable habitats for fungi by supplying space, food, and other chemicals stuff that in some cases is a reciprocal relationship or called mutualism symbiotic. Some marine invertebrates have interesting activities that are useful for human life such as anticancer, antifungal, and antibacterial. Many reports indicated that the fungal growth and their production of bioactive compounds were highly affected by the media or nutrition. In order to understand the effect of media on the number and bioactivity of the isolates, we collected the samples of marine invertebrates from two locations in Makassar. Invertebrate specimens were collected by hand during SCUBA diving at 3-10 m depths. The fungi were isolated by tapping method either on potato dextrose agar (PDA) or poor marine agar (PMA). The samples were collected from the Samalona water as much as 16 specimens that provided 30 and 18 fungal isolates on PDA and PMA, respectively, while, from the Barrang Cadi water, a total 14 specimens were collected to provide 12 and 3 isolates on PDA and PMA, respectively. All fungi from PMA inhibited the V. harveyi, V. vulnificus, and V. parahaemolyticus with weak, medium, and strong activities, while, the isolates from PDA were mostly not active against the Vibrios. Based on the molecular analyses, the active isolates were identified as Aspergillus flavus, A. oryzae, A. aculeatus, Talaromyces minioluteus, Hypocrea jecorina, Gliomastix murorum, Myrothecium inundatum, and Curvularia avinis. In conclusion, the isolates from PMA showed higher potential as source of antivibrio substances.
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References
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Chen, L., Hu, J. S., Xu, J. L., Shao, C. L. and Wang, G. Y. (2018) ‘Biological and chemical diversity of ascidian-associated microorganisms’, Marine Drugs, 16(10), pp. 1–33. doi: 10.3390/md16100362.
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Pham, J. V., Yilma, M. A., Feliz, A., Majid, M. T., Maffetone, N., Walker, J. R., Kim, E., Cho, H. J., Reynolds, J. M., Song, M. C., Park, S. R. and Yoon, Y. J. (2019) ‘A review of the microbial production of bioactive natural products and biologics’, Frontiers in Microbiology, 10(JUN), pp. 1–27. doi: 10.3389/fmicb.2019.01404.
Rani, N. and Jain, P. (2017) ‘Isolation of antimicrobial compound producing fungi from the rhizospheric soil of the medicinal plant Azadirachta indica’, ournal of Chemical and Pharmaceutical Research, 9(9), pp. 265–270.
Ruiz, B., Chávez, A., Forero, A., García-Huante, Y., Romero, A., Snchez, M., Rocha, D., Snchez, B., Rodríguez-Sanoja, R., Sánchez, S. and Langley, E. (2010) ‘Production of microbial secondary metabolites: Regulation by the carbon source’, Critical Reviews in Microbiology, 36(2), pp. 146–167. doi: 10.3109/10408410903489576.
Schmoll, M. and Kubicek, Æ. C. P. (2005) ‘ooc1 , a unique gene expressed only during growth of Hypocrea jecorina ( anamorph?: Trichoderma reesei ) on cellulose’, pp. 126–133. doi: 10.1007/s00294-005-0585-1.
Sharma, G. and Pandey, R. R. (2010) ‘Influence of culture media on growth, colony character and sporulation of fungi isolated from decaying vegetable wastes’, Journal of Yeast and Fungal Research, 1(8), pp. 157–164.
Sibero, M. T., Igarashi, Y., Radjasa, O. K., Sabdono, A., Trianto, A., Zilda, D. S. and Wijaya, Y. J. (2019) ‘Sponge-associated fungi from a mangrove habitat in Indonesia?: species composition , antimicrobial activity , enzyme screening and bioactive profiling’, International Aquatic Research. Springer Berlin Heidelberg, 11(2), pp. 173–186. doi: 10.1007/s40071-019-0227-8.
Sibero, M. T., Radjasa, O. K., Sabdono, A., Trianto, A., Triningsih, D. W. and Hutagaol, I. D. (2018) ‘Antibacterial activity of indonesian sponge associated fungi against clinical pathogenic multidrug resistant bacteria’, Journal of Applied Pharmaceutical Science, 8(2), pp. 088–094. doi: 10.7324/JAPS.2018.8214.
Sibero, M. T., Triningsih, D. W., Radjasa, O. K., Sabdono, A., Trianto, A., Priyani, N. and Prastyo, A. (2018) ‘Antimicrobial activity of sponge-associated fungi from Pandang Island, North Sumatera against clinical pathogenic microorganisms’, Asian Journal of Microbiology, Biotechnology and Environmental Sciences, 20(1), pp. 142–149.
Tarman, K., Lindequist, U., Wende, K., Porzel, A., Arnold, N. and Wessjohann, L. A. (2011) ‘Isolation of a new natural product and cytotoxic and antimicrobial activities of extracts from fungi of Indonesian marine habitats’, Marine Drugs, 9(3), pp. 294–306. doi: 10.3390/md9030294.
Tarman, K., Palm, G. J., Porzel, A., Merzweiler, K., Arnold, N., Wessjohann, L. A., Unterseher, M. and Lindequist, U. (2012) ‘Helicascolide C, a new lactone from an Indonesian marine algicolous strain of Daldinia eschscholzii (Xylariaceae, Ascomycota)’, Phytochemistry Letters. Phytochemical Society of Europe, 5(1), pp. 83–86. doi: 10.1016/j.phytol.2011.10.006.
Trianto, A., Sabdono, A., Rochaddi, B. and Triningsih, D. W. (2017) ‘Exploration of marine sponges- associated fungi producing antifungal’, Asian Journal of Microbiology, Biotechnology and Environmental Science, 19(3), pp. 588–593.
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De Voogd, N. J., Cleary, D. F. R., Hoeksema, B. W., Noor, A. and Van Soest, R. W. M. (2006) ‘Sponge beta diversity in the Spermonde Archipelago, SW Sulawesi, Indonesia’, Marine Ecology Progress Series, 309, pp. 131–142. doi: 10.3354/meps309131.
Wang, H.; Liu, L.; Guo, Y.-X.; Dong, Y.-S.; Zhang, D.-J.; Xiu, Z.-L. (2007). “Biotransformation of piceid in Polygonum cuspidatum to resveratrol by Aspergillus oryzae”. Applied Microbiology and Biotechnology. 75 (4): 763-768.
Xu, W., Guo, S., Gong, L., Alias, S. A., Pang, K. L. and Luo, Z. H. (2018) ‘Phylogenetic survey and antimicrobial activity of cultivable fungi associated with five scleractinian coral species in the South China Sea’, Botanica Marina, 61(1), pp. 75–84. doi: 10.1515/bot-2017-0005.
Xu, W., Guo, S., Gong, L. F., He, G., Pang, K. L. and Luo, Z. H. (2018) ‘Cultivable fungal diversity in deep-sea sediment of the East Pacific Ocean’, Geomicrobiology Journal. Informa UK Limited, trading as Taylor & Francis Group, 35(9), pp. 790–797. doi: 10.1080/01490451.2018.1473531.
Yanagihara, M., Kawasaki, M., Ishizaki, H. and Anzawa, K. (2010) ‘Tiny keratotic brown lesions on the interdigital web between the toes of a healthy man caused by Curvularia species infection and a review of cutaneous Curvularia infections’, pp. 224–233. doi: 10.1007/s10267-009-0030-2.
Zhou, Y., Debbab, A., Wray, V., Lin, W., Schulz, B., Trepos, R., Pile, C., Hellio, C., Proksch, P. and Aly, A. H. (2014) ‘Marine bacterial inhibitors from the sponge-derived fungus Aspergillus sp.’, Tetrahedron Letters. Elsevier Ltd, 55(17), pp. 2789–2792. doi: 10.1016/j.tetlet.2014.02.062.
Bhattacharyya, P. N. and Jha, D. K. (2011) ‘Optimization of cultural condition affecting growth and improved bioactive metabolite production by a subsurface Aspergillus strain TSF 146’, International Journal of Applied Biology and Pharmaceutical Technology, 2(4), pp. 133–143.
Bovio, E., Garzoli, L., Poli, A., Luganini, A., Villa, P., Musumeci, R., Mccormack, G. P., Cocuzza, C. E., Gribaudo, G., Mehiri, M. and Varese, G. C. (2019) ‘Marine Fungi from the sponge grantia compressa: biodiversity, chemodiversity, and biotechnological potential’, Marine Drugs, 17(4). doi: 10.3390/md17040220.
Calabon, M. S., Sadaba, R. B. and Campos, W. L. (2018) ‘Fungal diversity of mangrove-associated sponges from New Washington, Aklan, Philippines’, Mycology. Taylor & Francis, 0(0), pp. 1–16. doi: 10.1080/21501203.2018.1518934.
Carroll, A. R., Copp, B. R., Davis, R. A., Keyzers, R. A. and Prinsep, M. R. (2019) ‘Marine natural products’, Natural Product Reports, 36(1), pp. 122–173. doi: 10.1039/c8np00092a.
Chen, L., Hu, J. S., Xu, J. L., Shao, C. L. and Wang, G. Y. (2018) ‘Biological and chemical diversity of ascidian-associated microorganisms’, Marine Drugs, 16(10), pp. 1–33. doi: 10.3390/md16100362.
Demain, A. L. (1998) ‘Induction of microbial secondary metabolism’, International Microbiology, 1(4), pp. 259–264. doi: 10.2436/im.v1i4.26.
Grossart, H. P., Wurzbacher, C., James, T. Y. and Kagami, M. (2016) ‘Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi’, Fungal Ecology. Elsevier Ltd, 19, pp. 28–38. doi: 10.1016/j.funeco.2015.06.004.
Haris, A., Werorilangi, S., Gosalam, S. and Masâ€TMud, A. (2014) ‘Komposisi jenis dan kepadatan sponge (Porifera: Demospongiae) di Kepulauan Spermonde Kota Makassar’, Journal of Biota, 19(1). doi: 10.24002/biota.v19i1.453.
Hassett, B. T. and Gradinger, R. (2016) ‘Chytrids dominate arctic marine fungal communities’, Environmental Microbiology, 18(6), pp. 2001–2009. doi: 10.1111/1462-2920.13216.
Henríquez, M., Vergara, K., Norambuena, J., Beiza, A., Maza, F., Ubilla, P., Araya, I., Chávez, R., San-Martín, A., Darias, J., Darias, M. J. and Vaca, I. (2014) ‘Diversity of cultivable fungi associated with Antarctic marine sponges and screening for their antimicrobial, antitumoral and antioxidant potential’, World Journal of Microbiology and Biotechnology, 30(1), pp. 65–76. doi: 10.1007/s11274-013-1418-x.
Imhoff, J. F. (2016) ‘Natural products from marine fungi - still an underrepresented resource’, Marine Drugs, 14(1). doi: 10.3390/md14010019.
Jain, P. and Gupta, S. (2012) ‘Effect of carbon and nitrogen sources on antimicrobial metabolite production by endophytic fungus Penicillum sp. against human pathogens.’, Journal of Pharmacy Research, 5(8), pp. 4325–4328.
Jie, M. Z., Jiang, L. C., Di, Y. S. D. and Crews, P. (2016) ‘The Bioactive Secondary Metabolites from Talaromyces species’, Natural Products and Bioprospecting. Springer Berlin Heidelberg, 6(1), pp. 1–24. doi: 10.1007/s13659-015-0081-3.
Künzler, M. (2018) ‘How fungi defend themselves against microbial competitors and animal predators’, PLoS Pathogens. doi: 10.1371/journal.ppat.1007184.
Lindequist, U. (2016) ‘Marine-derived pharmaceuticals - challenges and opportunities’, Biomolecules and Therapeutics, 24(6), pp. 561–571. doi: 10.4062/biomolther.2016.181.
Litaay, M. (2018) ‘Marine tunicates from Sangkarang Archipelago Indonesia: Recent finding and bio-prospecting’, Journal of Physics: Conference Series, 979(1). doi: 10.1088/1742-6596/979/1/012003.
Litaay, M., Santosa, S., Johannes, E., Agus, R., Moka, W., Dhewi, J. and Tanjung, D. (2018) ‘Biodiversity of marine tunicates in Samalona waters, Sangkarang Archipelago, Indonesia’, Spermonde, 4(1), pp. 26–31.
Muggia, L., Kopun, T. and Grube, M. (2017) ‘Effects of growth media on the diversity of culturable fungi from lichens’, Molecules, 22(5), pp. 1–22. doi: 10.3390/molecules22050824.
Nemeth, J., Oesch, G. and Kuster, S. P. (2015) ‘Bacteriostatic versus bactericidal antibiotics for patients with serious bacterial infections: systematic review and meta-analysis’, Journal of Antimicrobial Chemotherapy, 70, pp. 382–395. doi: 10.1093/jac/dku379.
Pereira, F. (2019) ‘Have marine natural product drug discovery efforts been productive and how can we improve their efficiency?’, Expert Opinion on Drug Discovery. Taylor & Francis, 14(8), pp. 717–722. doi: 10.1080/17460441.2019.1604675.
Pham, J. V., Yilma, M. A., Feliz, A., Majid, M. T., Maffetone, N., Walker, J. R., Kim, E., Cho, H. J., Reynolds, J. M., Song, M. C., Park, S. R. and Yoon, Y. J. (2019) ‘A review of the microbial production of bioactive natural products and biologics’, Frontiers in Microbiology, 10(JUN), pp. 1–27. doi: 10.3389/fmicb.2019.01404.
Rani, N. and Jain, P. (2017) ‘Isolation of antimicrobial compound producing fungi from the rhizospheric soil of the medicinal plant Azadirachta indica’, ournal of Chemical and Pharmaceutical Research, 9(9), pp. 265–270.
Ruiz, B., Chávez, A., Forero, A., García-Huante, Y., Romero, A., Snchez, M., Rocha, D., Snchez, B., Rodríguez-Sanoja, R., Sánchez, S. and Langley, E. (2010) ‘Production of microbial secondary metabolites: Regulation by the carbon source’, Critical Reviews in Microbiology, 36(2), pp. 146–167. doi: 10.3109/10408410903489576.
Schmoll, M. and Kubicek, Æ. C. P. (2005) ‘ooc1 , a unique gene expressed only during growth of Hypocrea jecorina ( anamorph?: Trichoderma reesei ) on cellulose’, pp. 126–133. doi: 10.1007/s00294-005-0585-1.
Sharma, G. and Pandey, R. R. (2010) ‘Influence of culture media on growth, colony character and sporulation of fungi isolated from decaying vegetable wastes’, Journal of Yeast and Fungal Research, 1(8), pp. 157–164.
Sibero, M. T., Igarashi, Y., Radjasa, O. K., Sabdono, A., Trianto, A., Zilda, D. S. and Wijaya, Y. J. (2019) ‘Sponge-associated fungi from a mangrove habitat in Indonesia?: species composition , antimicrobial activity , enzyme screening and bioactive profiling’, International Aquatic Research. Springer Berlin Heidelberg, 11(2), pp. 173–186. doi: 10.1007/s40071-019-0227-8.
Sibero, M. T., Radjasa, O. K., Sabdono, A., Trianto, A., Triningsih, D. W. and Hutagaol, I. D. (2018) ‘Antibacterial activity of indonesian sponge associated fungi against clinical pathogenic multidrug resistant bacteria’, Journal of Applied Pharmaceutical Science, 8(2), pp. 088–094. doi: 10.7324/JAPS.2018.8214.
Sibero, M. T., Triningsih, D. W., Radjasa, O. K., Sabdono, A., Trianto, A., Priyani, N. and Prastyo, A. (2018) ‘Antimicrobial activity of sponge-associated fungi from Pandang Island, North Sumatera against clinical pathogenic microorganisms’, Asian Journal of Microbiology, Biotechnology and Environmental Sciences, 20(1), pp. 142–149.
Tarman, K., Lindequist, U., Wende, K., Porzel, A., Arnold, N. and Wessjohann, L. A. (2011) ‘Isolation of a new natural product and cytotoxic and antimicrobial activities of extracts from fungi of Indonesian marine habitats’, Marine Drugs, 9(3), pp. 294–306. doi: 10.3390/md9030294.
Tarman, K., Palm, G. J., Porzel, A., Merzweiler, K., Arnold, N., Wessjohann, L. A., Unterseher, M. and Lindequist, U. (2012) ‘Helicascolide C, a new lactone from an Indonesian marine algicolous strain of Daldinia eschscholzii (Xylariaceae, Ascomycota)’, Phytochemistry Letters. Phytochemical Society of Europe, 5(1), pp. 83–86. doi: 10.1016/j.phytol.2011.10.006.
Trianto, A., Sabdono, A., Rochaddi, B. and Triningsih, D. W. (2017) ‘Exploration of marine sponges- associated fungi producing antifungal’, Asian Journal of Microbiology, Biotechnology and Environmental Science, 19(3), pp. 588–593.
Trianto, A., Sabdono, A., Rochaddi, B., Triningsih, D. W. and Zilda, D. S. (2018) ‘Identification sponges-associated fungi from Karimunjawa National Park’, IOP Conference Series: Earth and Environmental Science, 116(1). doi: 10.1088/1755-1315/116/1/012098.
De Voogd, N. J., Cleary, D. F. R., Hoeksema, B. W., Noor, A. and Van Soest, R. W. M. (2006) ‘Sponge beta diversity in the Spermonde Archipelago, SW Sulawesi, Indonesia’, Marine Ecology Progress Series, 309, pp. 131–142. doi: 10.3354/meps309131.
Wang, H.; Liu, L.; Guo, Y.-X.; Dong, Y.-S.; Zhang, D.-J.; Xiu, Z.-L. (2007). “Biotransformation of piceid in Polygonum cuspidatum to resveratrol by Aspergillus oryzae”. Applied Microbiology and Biotechnology. 75 (4): 763-768.
Xu, W., Guo, S., Gong, L., Alias, S. A., Pang, K. L. and Luo, Z. H. (2018) ‘Phylogenetic survey and antimicrobial activity of cultivable fungi associated with five scleractinian coral species in the South China Sea’, Botanica Marina, 61(1), pp. 75–84. doi: 10.1515/bot-2017-0005.
Xu, W., Guo, S., Gong, L. F., He, G., Pang, K. L. and Luo, Z. H. (2018) ‘Cultivable fungal diversity in deep-sea sediment of the East Pacific Ocean’, Geomicrobiology Journal. Informa UK Limited, trading as Taylor & Francis Group, 35(9), pp. 790–797. doi: 10.1080/01490451.2018.1473531.
Yanagihara, M., Kawasaki, M., Ishizaki, H. and Anzawa, K. (2010) ‘Tiny keratotic brown lesions on the interdigital web between the toes of a healthy man caused by Curvularia species infection and a review of cutaneous Curvularia infections’, pp. 224–233. doi: 10.1007/s10267-009-0030-2.
Zhou, Y., Debbab, A., Wray, V., Lin, W., Schulz, B., Trepos, R., Pile, C., Hellio, C., Proksch, P. and Aly, A. H. (2014) ‘Marine bacterial inhibitors from the sponge-derived fungus Aspergillus sp.’, Tetrahedron Letters. Elsevier Ltd, 55(17), pp. 2789–2792. doi: 10.1016/j.tetlet.2014.02.062.
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