Abstract
Marine actinobacteria particularly from marine environments are believed to be inexhaustible sources of biologically active molecules for biomedical and industrial applications. We isolated 126 strains of marine actinomycetes from marine invertebrates such as corals, sponges and gastropod molluscs from Daya Bay and Nansha Islands. The chemical diversity of the metabolites from the isolated strains was evaluated using HPLC-UV fingerprinting and their antibacterial activity was estimated. Preliminary chemical screening and antibacterial activity clearly illustrate that the marine invertebrates-associated actinomycetes are a rich source of novel biologically active compounds. Among the isolates, strain SCSIO-PTE-L054 was further investigated for its unique metabolic profile and antibacterial activity. The bioassay-guided isolation rendered a polycyclic tetramate macrolactam (PTM) as a major chemical constituent with potent antibacterial activity. Our results revealed that the Streptomyces sp., strain SCSIO-L054 is a new source of PTMs which could pave a way to isolation of new series of PTMs with a broad spectrum of activity. In summary, the present investigation makes it possible to select marine actinomycetes from Daya Bay and Nansha Islands as new potential sources to produce potent compounds for a wide range of applications in future drug discovery.






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REFERENCES
Abdelfattah, M.S., Elmallah, M.I.Y., Hawas, U.W., El-Kassema, L.T.A., and, Eid M.A.G., Isolation and characterization of marine-derived actinomycetes with cytotoxic activity from the Red Sea coast, Asian Pac. J. Trop. Biomed., 2016, vol. 6, pp. 651–657.
Balouiri, M., Sadiki, M., and Ibnsouda, S.K., Methods for in vitro evaluating antimicrobial activity: a review, J. Pharm. Anal., 2016, vol. 6, pp. 71–79.
Baltz, R.H., Marcel Faber Roundtable: is our antibiotic pipeline unproductive because of starvation, constipation or lack of inspiration?, J. Ind. Microbiol. Biotechnol., 2006, vol. 33, pp. 507–513.
Carrano, L. and Marinelli, F., The relevance of chemical dereplication in microbial natural product screening, J. App. Bioanal., 2015, vol. 1, pp. 55–67.
Cumsille, A., Undabarrena, A., González, V., Claverías, F., Rojas, C., and Cámara, B., Biodiversity of Actinobacteria from the South Pacific and the assessment of Streptomyces chemical diversity with metabolic profiling, Mar. Drugs., 2017, vol. 15, p. 286.
D’Costa., V.M., King, C.E., Kalan, L., Morar, M., Sung., W.W.L., Schwarz, C., Froese, D., Zazula, G., Calmels, F., Debruyne, R., Golding, G.B., Poinar, H.N., and Wright, G.D., Antibiotic resistance is ancient, Nature, 2011, vol. 477, p. 457.
Dharmaraj, S., Marine Streptomyces as a novel source of bioactive substances, World J. Microb. Biot., 2010, vol. 26, no. 12, pp. 2123−2139.
Fatahi-Bafghi, M., Rasouli-nasab, M., Yasliani-Fard, S., Habibnia, S., Gharehbaghi, F., Eshraghi, S.S., and Heidarieh, P., Diversity and antimicrobial activity of actinomycetes isolated from Lut Desert: the extremely arid climatic zones of Iran, Int. J. Pept. Res. Ther., 2019, vol. 25, no. 3, pp. 1201–1207.
Fguira, L.F.B., Fotso, S., Ameur-Mehdi, R.B., Mellouli, L., and Laatsch, H, Purification and structure elucidation of antifungal and antibacterial activities of newly isolated Streptomyces sp. strain US80, Res. Microbiol., 2005, vol. 156, pp. 341–347.
Hentschel, U., Fieseler, L., Wehrl, M., Gernert, C., Steinert, M., Hacker, J., and Horn, M., Microbial diversity of marine sponges, in Sponges (Porifera), Springer, 2003, pp 59–88.
Jenkins, R., Burton, N., and Cooper, R., Effect of manuka honey on the expression of universal stress protein A in meticillin-resistant Staphylococcus aureus,Int. J. Antimicrob. Agents, 2011, vol. 37, pp. 373–376.
Jomon, K., Kuroda, Y., Ajisaka, M., and Sakai, H., A new antibiotic, ikarugamycin, J. Antibiot. 1972, vol. 25, no. 5, pp. 271–280.
Kalyani, B.S., Krishna, P., and Sreenivasulu, K., Screening and identification of novel isolate Streptomyces sp., NLKPB45 from Nellore costal region for its biomedical applications, Saudi J. Biol. Sci. 2019, vol. 26, no. 7, pp. 655–1660.
Kim, D.G., Moon, K., Kim, S.H., Park, S.H., Park, S., Lee, S.K., Oh, K.B., Shin, J., and Oh, D.C., Bahamaolides A and B, antifungal polyene polyol macrolides from the marine actinomycete Streptomyces sp., J. Nat. Prod., 2012, vol. 75, pp. 959–967.
Kong, F. and Carter, G.T., Structure determination of glycinocins A to D, further evidence for the cyclic structure of the amphomycin antibiotics, J. Antibiot., 2003, vol. 56, pp. 557–564.
Kumar, P.S., Duraipandiyan, V., and Ignacimuthu, S., Isolation, screening and partial purification of antimicrobial antibiotics from soil Streptomyces sp. SCA 7, Kaohsiung J. Med. Sci., 2014, vol. 30, pp. 435–446.
Kumar, P.S., Stalin, A., Duraipandiyan, V., Al-Dhabi, N.A., Yuvaraj, P., Balakrishna, K., and Ignacimuthu, S., Isolation of chemical constituents from Nonomuraea species: in vitro and in silico evaluation of its antibacterial properties, Beni-Seuf Univ.J. Bas. Appl. Sci., 2017, vol. 6, pp. 15–23.
Lacret, R., Oves-Costales, D., Gómez, C., Díaz, C., de la Cruz, M., Pérez-Victoria, I., Vicente, F., Genilloud, O., and Reyes, F., New ikarugamycin derivatives with antifungal and antibacterial properties from Streptomyces zhaozhouensis,Mar. Drugs, 2015, vol. 13, pp. 128–140.
Lin, H.N., Wang, K.L., Wu, Z.H., Tian, R.M., Liu, G.Z., and Xu, Y., Biological and chemical diversity of bacteria associated with a marine flatworm, Mar. Drugs, 2017, vol. 15, p. 281.
Mo, X., Li, Q., and Ju, J., Naturally occurring tetramic acid products: isolation, structure elucidation and biological activity, RSC Adv., 2014, vol. 4, pp. 50566–50593.
Nagashima, K., Shimizu, T., Takeshi, K., Kawakami, M., Yasokawa, D., Nakagawa, R., and Okumura, Y., A simple and sensitive polymerase chain reaction method for the detection of food-related bacteria, Food Sci. Technol. Res., 2007, vol. 6, no. 2, pp. 115–118.
Nolte, E. and McKee, C.M., Measuring the health of nations: updating an earlier analysis, Health Affairs, 2008, vol. 27, pp. 58–71.
Peraud, O., Biggs, J.S, Hughen, R.W., Light, A.R., Concepcion, G.P., Olivera, B.M., and Schmidt, E.W., Microhabitats within venomous cone snails contain diverse actinobacteria, Appl. Environ. Microbiol., 2009, vol. 75, pp. 6820–6826.
Ramasamy, P., Vino, A.B., Saravanan, R., Subhapradha, N., Shanmugam, V., and Shanmugam, A., Screening of antimicrobial potential of polysaccharide from cuttlebone and methanolic extract from body tissue of Sepia prashadi Winkworth, 1936, Asian Pac. J. Trop. Biomed., 2011, vol. 1, pp. S244–S248.
Rather, S.A., Shah, A.M., Ali, S.A., Dar, R.A., Rah, B., Ali, A., and Hassan, Q.P., Isolation and characterization of Streptomyces tauricus from Thajiwas glacier—a new source of actinomycin D, Med. Chem. Res., 2017, vol. 26, pp. 1897–1902.
Saha, S., Zhang, W., Zhang, G., Zhu, Y., Chen, Y., Liu, W., Yuan, C., Zhang, Q., Zhang, H., Zhang, L., Zhang, W., and Zhang, C., Activation and characterization of a cryptic gene cluster reveals a cyclization cascade for polycyclic tetramate macrolactams, Chem. Sci., 2017, vol. 8, pp. 1607–1612.
Sujatha, P., Raju, K. B., and Ramana, T., Studies on a new marine streptomycetes BT-408 producing polyketide antibiotic SBR-22 effective against methicillin resistant Staphylococcus aureus.Microbiol. Res., 2005, vol. 160, no. 2, pp. 119–126.
Takagi, M. and Shin-ya, K., Construction of a natural product library containing secondary metabolites produced by actinomycetes, J. Antibiot., 2012, vol. 65, p. 443.
Taylor, M.W., Schupp, P.J., De Nys, R., Kjelleberg, S., and Steinberg, P.D., Biogeography of bacteria associated with the marine sponge Cymbastela concentrica,Environ. Microbiol., 2005, vol. 7, pp. 419–433.
Wang, X., Zhang, M., Gao, J., Pu, T., Bilal, M., Wang, Y., and Zhang, X., Antifungal activity screening of soil actinobacteria isolated from Inner Mongolia, China, Biol. Control., 2018, vol. 127, pp. 78–84.
Xu, D., Han, L., Li, C., Cao, Q., Zhu, D., Barrett, N.H., Harmody, D., Chen, J., Zhu, H., McCarthy, P.J., Sun, X., and Wang, G., Bioprospecting deep-sea Actinobacteria for novel anti-infective natural products, Front. Microbiol., 2018, vol. 9, p. 787.
Yu, J., Zhang, L., Liu, Q., Qi, X., Ji, Y., and Kim, B.S., Isolation and characterization of actinobacteria from Yalujiang coastal wetland, North China, Asian Pac. J. Trop. Biomed., 2015, vol. 5, pp. 555–560.
Yuan, G.J., Li, P.B., Yang, H., Wu, X.Y., Tu, G.Q., and Wei, S.J., Chemical screening of sixty-one actinomycete strains and anti-methicillin-resistant Staphylococcus aureus assays of target strains, CJNM., 2012, vol. 10, no. 2, pp. 155–160.
Zhang, L., Integrated approaches for discovering novel drugs from microbial natural products, in Natural Products, Springer, 2005, pp 33–55.
Zhang, Q., Li, S., Chen, Y., Tian, X., Zhang, H., Zhang, G., Zhu, Y., Zhang, S., Zhang, W., Zhang, C., New diketopiperazine derivatives from a deep-sea-derived Nocardiopsis alba SCSIO 03039, J. antibiot., 2013, vol. 66, p. 31.
Zhang, W., Zhang, G., Zhang, L., Liu, W., Jiang, X., Jin, H., Liu, Z., Zhang, H.B., Zhou, A., and Zhang, C., New polycyclic tetramate macrolactams from marine-derived Streptomyces sp. SCSIO 40060, Tetrahedron., 2018, vol. 74, pp. 6839–6845.
Zhang, X., Du, J., Wang, Y., Chen, S., and Wang, Y., Escherichiacoli GutM4 produces 2,5-diketopiperazines and inhibits human pathogens in vitro, Electron. J. Biotechnol., 2017, vol. 28, pp. 35–40.
Zheng, X., Wang, J., Chen, Z., Zhang, H., Wang, Z., Zhu, Y., and Liu, B. A Streptomyces sp. strain: isolation, identification, and potential as a biocontrol agent against soilborne diseases of tomato plants, Biol. Control., 2019, vol. 136, p. 104004.
ACKNOWLEDGMENTS
We thank Mrs Aijun Sun, Dr Xiaohong Zheng, Ms Yun Zhang and Dr Zhihui Xiao in the analytical facility center of the SCSIO for recording MS and NMR data.
Funding
This work was supported by the National Natural Science Foundation of China (41706169, U1501223 and U1706206), the Chinese Academy of Sciences (XDA13020302) and Natural Science Foundation of Guangdong Province (2016A030312014).
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Kumar, P.S., Ling, C.Y., Zhou, Z.B. et al. Chemical Diversity of Metabolites and Antibacterial Potential of Actinomycetes Associated with Marine Invertebrates from Intertidal Regions of Daya Bay and Nansha Islands. Microbiology 89, 483–492 (2020). https://doi.org/10.1134/S0026261720040062
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DOI: https://doi.org/10.1134/S0026261720040062

