Abstract
Marine symbiotic fungi represent an intriguing source of discovery of novel secondary metabolites with various biological activities. Sea anemones are benthic marine invertebrates, however, the cultivable symbiotic fungi residing in the sea anemones are paid few attentions compared to those derived from their cnidarian counterparts. Here we show the identification of antimicrobial secondary metabolites from the sea anemone-derived symbiotic fungi. Out of five isolated fungal strains, only the strain SMA01 showed strong antimicrobial activities, which was assigned into the genus Emericella based on the morphological characteristics and the ITS sequencing. Media swift from liquid fermentation to solid rice medium presented little influence on its antibacterial activity. A chemical investigation of the ethyl acetate extract of the Emericella sp. SMA01 led to discovery of the primary antibiotic metabolite phenazine-1-carboxylic acid. The IC50 values of the phenazine-1-carboxylic acid against Phytophthora capsici, Gibberella zeae, and Verticillium dahliae were determined to be 23.26–53.89 µg/mL. To the best of our knowledge, this was the first report of Emericella sp. in sea anemones. The current study may benefit understanding of the defensive chemical interactions between the symbiotic fungi and their host sea anemones.
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Data Availability Statement
The datasets analyzed during the current study are available from the corresponding author on reasonable request.
References
Amend A S, Barshis D J, Oliver T A. 2012. Coral-associated marine fungi form novel lineages and heterogeneous assemblages. The ISME Journal, 6(7): 1 291–1 301, https://doi.org/10.1038/ismej.2011.193.
Bolaños J, De León L F, Ochoa E, Darias J, Raja H A, Shearer C A, Miller A N, 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. Marine Biotechnology, 17(5): 533–564, https://doi.org/10.1007/s10126-015-9634-z.
Bugni T S, Ireland C M. 2004. Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Natural Product Reports, 21(1): 143–163, https://doi.org/10.1039/b301926h.
Calabon M S, Sadaba R B, Campos W L. 2019. Fungal diversity of mangrove-associated sponges from New Washington, Aklan, Philippines. Mycology, 10(1): 6–21, https://doi.org/10.1080/21501203.2018.1518934.
Carroll A R, Copp B R, Davis R A, Keyzers R A, Prinsep M R. 2020. Marine natural products. Natural Product Reports, 37(2): 175–223, https://doi.org/10.1039/C9NP00069K.
Chen H Y, Liu T K, Yang J, Yang X L. 2019. Emerones A-C: three novel merosesquiterpenoids with unprecedented skeletons from Emericella sp. XL029. Organic & Biomolecular Chemistry, 17(36): 8 450–8 455, https://doi.org/10.1039/C9OB01788G.
Chen L, Hu J S, Xu J L, Shao C L, Wang G Y. 2018. Biological and chemical diversity of ascidian-associated microorganisms. Marine Drugs, 16(10): 362, https://doi.org/10.3390/md16100362.
Da Silva M, Passarini M R Z, Bonugli R C, Sette L D. 2008. Cnidarian-derived filamentous fungi from Brazil: isolation, characterisation and RBBR decolourisation screening. Environmental Technology, 29(12): 1 331–1 339, https://doi.org/10.1080/09593330802379466.
Fredimoses M, Zhou X F, Ai W, Tian X P, Yang B, Lin X P, Liu J, Liu Y H. 2019. Emerixanthone E, a new xanthone derivative from deep sea fungus Emericella sp SCSIO 05240. Natural Product Research, 33(14): 2 088–2 094, https://doi.org/10.1080/14786419.2018.1487966.
Guillen P O, Jaramillo K B, Genta-Jouve G. 2020. Marine natural products from zoantharians: bioactivity, biosynthesis, systematics, and ecological roles. Natural Product Reports, 37(4): 515–540, https://doi.org/10.1039/C9NP00043G.
He Y, Hu Z X, Li Q, Huang J F, Li X N, Zhu H C, Liu J J, Wang J P, Wang J P, Xue Y B, Zhang Y H. 2017. Bioassay-guided isolation of antibacterial metabolites from Emericella sp. TJ29. Journal of Natural Products, 80(9): 2 399–2 405, https://doi.org/10.1021/acs.jnatprod.7b00077.
Jayatilake G S, Thornton M P, Leonard A C, Grimwade J E, Baker B J. 1996. Metabolites from an Antarctic sponge-associated bacterium, Pseudomonas aeruginosa. Journal of Natural Products, 59(3): 293–296, https://doi.org/10.1021/np960095b.
Jones E B G, Stanley S J, Pinruan U. 2008. Marine endophyte sources of new chemical natural products: a review. Botanica Marina, 51(3): 163–170, https://doi.org/10.1515/BOT.2008.028.
León-Palmero E, Joglar V, Álvarez P A, Martín-Platero A, Llamas I, Reche I. 2018. Diversity and antimicrobial potential in sea anemone and holothurian microbiomes. PLoS One, 13(5): e0196178, https://doi.org/10.1371/journal.pone.0196178.
Li Q, Chen C M, Cheng L, Wei M S, Dai C, He Y, Gong J J, Zhu R Q, Li X N, Liu J J, Wang J P, Zhu H C, Zhang Y H. 2019. Emeridones A-F, a series of 3,5-demethylorsellinic acid-based meroterpenoids with rearranged skeletons from an endophytic fungus Emericella sp. TJ29. The Journal of Organic Chemistry, 84(3): 1 534–1 541, https://doi.org/10.1021/acs.joc.8b02830.
Liu C L, Tian L, Li G Y. 2001. The fungi from anemones in the intertidal zone of Qingdao sea area and the antimicrobial substance they produced. Chinese Journal of Marine Drugs, 20(6): 1–3, https://doi.org/10.3969/j.issn.1002-3461.2001.06.001. (in Chinese with English abstract)
Liu S, Ahmed S, Zhang C G, Liu T X, Shao C L, Fang Y W. 2020. Diversity and antimicrobial activity of culturable fungi associated with sea anemone Anthopleura xanthogrammica. Electronic Journal of Biotechnology, 44: 41–46, https://doi.org/10.1016/j.ejbt.2020.01.003.
López-Legentil S, Erwin P M, Turon M, Yarden O. 2015. Diversity of fungi isolated from three temperate ascidians. Symbiosis, 66(2): 99–106, https://doi.org/10.1007/s13199-015-0339-x.
Malmstrøm J, Christophersen, C, Barrero A F, Oltra J E, Justicia J, Rosales A. 2002. Bioactive metabolites from a marine-derived strain of the fungus Emericella variecolor. Journal of Natural Products, 65(3): 364–367, https://doi.org/10.1021/np0103214.
Malmstrøm J. 1999. Unguisins A and B: new cyclic peptides from the marine-derived fungus Emericella unguis. Journal of Natural Products, 62(5): 787–789, https://doi.org/10.1021/np980539z.
Mavrodi D V, Blankenfeldt W, Thomashow L S. 2006. Phenazine compounds in fluorescent Pseudomonas spp. Biosynthesis and regulation. Annual Review of Phytopathology, 44: 417–445, https://doi.org/10.1146/annurev.phyto.44.013106.145710.
Nithyanand P, Indhumathi T, Ravi A V, Pandian S K. 2011. Culture independent characterization of bacteria associated with the mucus of the coral Acropora digitifera from the Gulf of Mannar. World Journal of Microbiology and Biotechnology, 27(6): 1 399–1 406, https://doi.org/10.1007/s11274-010-0591-4.
Oh D C, Kauffman C A, Jensen P R, Fenical W. 2007. Induced production of Emericellamides A and B from the marine-derived fungus Emericella sp. in competing co-culture. Journal of Natural Products, 70(4): 515–520, https://doi.org/10.1021/np060381f.
Pang X J, Zhang S B, Chen H L, Zhao W T, Yang D E, Xian P J, Xu L L, Tao Y D, Fu H Y, Yang X L. 2018. Emericelactones A-D: four novel polyketides produced by Emericella sp. XL 029, a fungus associated the leaves of Panax notoginseng. Tetrahedron Letters, 59(52): 4 566–4 570, https://doi.org/10.1016/j.tetlet.2018.11.032.
Paul V J, Arthur K E, Ritson-Williams R, Ross C, Sharp K. 2007. Chemical defenses: from compounds to communities. The Biological Bulletin, 213(3): 226–251, https://doi.org/10.2307/25066642.
Piel J. 2009. Metabolites from symbiotic bacteria. Natural Product Reports, 26(3): 338–362, https://doi.org/10.1039/B703499G.
Qin X Y, Yang K L, Li J, Wang C Y, Shao C L. 2015. Phylogenetic diversity and antibacterial activity of culturable fungi derived from the zoanthid Palythoa haddoni in the South China Sea. Marine Biotechnology, 17(1): 99–109, https://doi.org/10.1007/s10126-014-9598-4.
Rojko N, Dalla Serra M, Maček P, Anderluh G. 2016. Pore formation by actinoporins, cytolysins from sea anemones. Biochimica et Biophysica Acta (BBA) -Biomembranes, 1858(3):446–456,https://doi.org/10.1016/j.bbamem.2015.09.007.
Saleem M, Ali M S, Hussain S, Jabbar A, Ashraf M, Lee Y S. 2007. Marine natural products of fungal origin. Natural Product Reports, 24(5): 1 142–1 152, https://doi.org/10.1039/b607254m.
Schmidt E W, Donia M S, McIntosh J A, Fricke W F, Ravel J. 2012. Origin and variation of tunicate secondary metabolites. Journal of Natural Products, 75(2): 295–304, https://doi.org/10.1021/np200665k.
Schmidt E W. 2008. Trading molecules and tracking targets in symbiotic interactions. Nature Chemical Biology, 4(8): 466–473, https://doi.org/10.1038/nchembio.101.
Schmidt E. 2009. Bacterial chemical defenses of marine animal hosts. In: White Jr J F, Torres M S eds. Defensive Mutualism in Microbial Symbiosis. Boca Raton: CRC Press, 65–83, https://doi.org/10.1201/9781420069327.ch5.
Shnit-Orland M, Kushmaro A. 2009. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiology Ecology, 67(3): 371–380, https://doi.org/10.1111/j.1574-6941.2008.00644.x.
Thomashow L S, Weller D M, Bonsall R F, Pierson III L S. 1990. Production of the antibiotic phenazine-1-carboxylic Acid by fluorescent Pseudomonas species in the rhizosphere of wheat. Applied and Environmental Microbiology, 56(4): 908–912, https://doi.org/10.1128/AEM.56.4.908-912.1990.
Wang F, Tan J W, Liu J K. 2004. Vibratilicin: a novel compound from the basidiomycete Cortinarius vibratilis. Helvetica Chimica Acta, 87(7): 1 912–1 915, https://doi.org/10.1002/hlca.200490170.
Xu Y M, Espinosa-Artiles P, Liu M X, Arnold A E, Gunatilaka A A L. 2013. Secoemestrin D, a cytotoxic epitetrathiodioxopiperizine, and Emericellenes A-E, five sesterterpenoids from Emericella sp. AST0036, a fungal endophyte of Astragalus lentiginosus. Journal of Natural Products, 76(12): 2 330–2 336, https://doi.org/10.1021/np400762k.
Yang K L, Wei M Y, Shao C L, Fu X M, Guo Z Y, Zheng C J, She Z G, Lin Y C, Wang C Y. 2012. Antibacterial anthraquinone derivatives from a sea anemone-derived fungus Nigrospora sp. Journal of Natural Products, 75(5): 935–941, https://doi.org/10.1021/np300103w.
Yue Y, Yu H H, Li R F, Xing R G, Liu S, Li P C. 2015. Exploring the antibacterial and antifungal potential of jellyfish-associated marine fungi by cultivation-dependent approaches. PLoS One, 10(12): e0144394, https://doi.org/10.1371/journal.pone.0144394.
Zhang X Y, Bao J, Wang G H, He F, Xu X Y, Qi S H. 2012. Diversity and antimicrobial activity of culturable fungi isolated from six species of the South China Sea Gorgonians. Microbial Ecology, 64(3): 617–627, https://doi.org/10.1007/s00248-012-0050-x.
Zhang Y L, Li S, Jiang D H, Kong L C, Zhang P H, Xu J D. 2013. Antifungal activities of metabolites produced by a termite-associated Streptomyces canus BYB02. Journal of agricultural and Food Chemistry, 61(7): 1 521–1 524, https://doi.org/10.1021/Jf305210u.
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Supported by the National Natural Science Foundation of China (Nos. 41376004, 41406152), the Key Research and Development Project of Shandong Province (No. 2018GHY115008), the Youth Innovation Promotion Association of CAS, and the Scientific and Technological Innovation Project (No. 2015ASKJ02)
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Yue, Y., Yu, H., Li, R. et al. Isolation and identification of antimicrobial metabolites from sea anemone-derived fungus Emericella sp. SMA01. J. Ocean. Limnol. 39, 1010–1019 (2021). https://doi.org/10.1007/s00343-020-0203-6
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DOI: https://doi.org/10.1007/s00343-020-0203-6