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Culture Medium Optimization and Active Compounds Investigation of an Anti-Quorum Sensing Marine Actinobacterium Nocardiopsis dassonvillei JS106

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Abstract

Quorum sensing inhibitors (QSIs) can block the quorum sensing system and might be useful in therapy of drug-resistant bacterial infections. To explore the anti-quorum sensing actinomycetes from marine habitats, in this study, a marine actinobacterium exhibiting strong anti-quorum sensing activity was isolated from marine sediment and identified as Nocardiopsis dassonvillei JS106. Effects of different culture media on the bioactivity and metabolites production of JS106 were investigated by using single-factor and orthogonal experiments. The results showed that soybean meal and NaCl were two important factors in the culture medium, and could significantly affect both the bioactivity and metabolites production of JS106. By culturing in the optimized medium containing 10 g/L soluble starch, 10 g/L soybean meal, and 15 g/L NaCl at pH 6.5, both metabolites production and anti-quorum sensing activity of JS106 were significantly increased (302 and 241%, respectively) compared to the original condition. The culture liquid of JS106 also showed strong anti-biofilm activity against Staphylococcus aureus and Pseudomonas aeruginosa with the inhibition rate of 77.94 and 50.56% at the concentration of 20 vol %, while it did not inhibit the growth of planktonic cells. Questiomycin A and a new compound 2-hydroxyacetate-3-hydroxyacetamido-phenoxazine (HHP) were isolated and identified from the cultures of JS106. The anti-quorum sensing activities (IC50) of questiomycin A and HHP against violacein production by Chromobacterium violaceum 12472 were 6.82 and 23.59 μg/mL, respectively. The strong anti-quorum sensing activity of N. dassonvillei JS106 indicated that this strain and its active phenoxazine metabolites could have good potential in anti-quorum sensing related applications.

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REFERENCES

  1. Abed, N.N.E., Screening the Egyptian actinomycetes as candidates for anti-microbial compounds and identification of Nocardiopsis dassonvillei HBUM17483, Biosci. Res., 2017, vol. 14, pp. 427–445.

    Google Scholar 

  2. Chen, X.C., Chen, J.W., Yan, Y.C., Chen, S., Xu, X.W., Zhang, H.W., and Wang, H., Quorum sensing inhibitors from marine bacteria Oceanobacillus sp. XC22919, Nat. Prod. Res., 2019, vol. 33, pp. 1819–1823.

    Article  CAS  Google Scholar 

  3. Fu, P., Liu, P.P., Gong, Q.H., Wang, Y., Wang, P., and Zhu, W.M., α-Pyrones from the marine-derived actinomycete Nocardiopsis dassonvillei subsp. dassonvillei XG-8-1, RSC Adv., 2013, vol. 3, pp. 20726–20731.

    Article  CAS  Google Scholar 

  4. Gao, H.J., Chu, X., Wang, Y.W., Zhou, F., Zhao, K., Mu, Z.M., and Liu, Q.X., Media optimization for laccase production by Trichoderma harzianum ZF-2 using response surface methodology, J. Microbiol. Biotechnol., 2013, vol. 23, pp. 1757–1764.

    Article  CAS  Google Scholar 

  5. Haquea, S., Ahmadb, F., Dara, S.A., Jaweda, A., Mandala, R.K., Wahida, M., Lohanic, M., Khand, S., Singhe, V., and Akhterf, N., Developments in strategies for quorum sensing virulence factor inhibition to combat bacterial drug resistance, Microb. Pathogenesis, 2018, vol. 121, pp. 293–302.

    Article  Google Scholar 

  6. Igarashi, Y., Takagi, K., Kajiura, T., and Furumai, T., Glucosylquestiomycin, a novel antibiotic from Microbispora sp. TP-A0184: fermentation, isolation, structure determination, synthesis and biological activities, J. Antibiot., 1998, vol. 51, pp. 915–920.

    Article  CAS  Google Scholar 

  7. Kamarudheen, N., Naushad, T. and Bhaskara, and Rao, K.V., Biosynthesis, characterization and antagonistic applications of extracellular melanin pigment from marine Nocardiopsis sps, Ind. J. Pharm. Educ. Res., 2019, vol. 53, pp. S112–S119.

    Article  CAS  Google Scholar 

  8. Kozlovsky, A.G., Zhelifonova, V.P., Antipova, T.V., Adanin, V.M., Novikova, N.D., Deshevaya, E.A., Schlege, B., Dahse, H.M., Gollmik, F., and Grafe, U., Penicillium expansum, a resident fungal strain of the orbital complex mir, producing xanthocyllin X and questiomycin A, Appl. Biochem. Microbiol., 2004, vol. 40, pp. 291–295.

    Article  CAS  Google Scholar 

  9. Liu, S.R. and Zhang, W.R., Optimization of submerged culture conditions involving a developed fine powder solid seed for exopolysaccharide production by the medicinal mushroom Ganoderma lucidum, Food Sci. Biotechnol., 2019, vol. 28, pp. 1135–1145.

    Article  CAS  Google Scholar 

  10. Manivasagan, P., Kang, K.H., Sivakumar, K., Li-Chan, E.C.Y., Oh, H.M., and Kim, S.K., Marine actinobacteria: an important source of bioactive natural products, Environ. Toxicol. Pharmacol., 2014, vol. 38, pp. 172–188.

    Article  CAS  Google Scholar 

  11. Maskey, R.P., Li, F.C., Qian, S., Fiebig, H.H., and Laatsch, H., Chandrananimycin A-C: production of novel anticancer antibiotics from a marine Actinomadura sp. isolate M048 by variation of medium composition and growth conditions, J. Antibiot., 2003, vol. 56, pp. 622–629.

    Article  CAS  Google Scholar 

  12. Miao, L., Xu, J., Yao, Z.W., Jiang, Y., Zhou, H.R., Jiang, W., and Dong, K.M., The anti-quorum sensing activity and bioactive substance of a marine derived Streptomyces, Biotechnol. Biotecnol. Equip., 2017, vol. 31, pp. 1007–1015.

    Article  CAS  Google Scholar 

  13. Ni, N.T., Li, M.Y., Wang, J.F., and Wang, B.H., Inhibitors and antagonists of bacterial quorum sensing, Med. Res. Rev., 2009, vol. 23, pp. 65–124.

    Article  Google Scholar 

  14. Pan, S.H., Chen, G.G., Zeng, J.J., Cao, X.Y., Zheng, X., Zeng, W., and Liang, Z.Q., Fibrinolytic enzyme production from low-cost substrates by marine Bacillus subtilis: process optimization and kinetic modeling, Biochem. Eng. J., 2019, vol. 141, pp. 268–277.

    Article  CAS  Google Scholar 

  15. Polkade, A.C., Mantri, S.S., Patwekar, U.J., and Jangid, K., Quorum sensing: an under-explored phenomenon in the phylum actinobacteria, Front. Microbiol., 2016, vol. 7, p. 131.

    Article  Google Scholar 

  16. Priyanka, S., Jayashree, M., Shivani, R., Anwesha, S., Bhaskara, Rao K.V., and Arnold, E.I., Characterization and identification of antibacterial compound from marine actinobacteria: in vitro and in silico analysis, J. Infect. Public Health, 2019, vol. 12, pp. 83–89.

    Article  CAS  Google Scholar 

  17. Reading, N.C. and Sperandio, V., Quorum sensing: the many languages of bacteria, FEMS Microbiol. Lett., 2006, vol. 254, pp. 1–11.

    Article  CAS  Google Scholar 

  18. Remy, B., Mion, S., Plener, L., Elias, M., Chabriere, E., and Daude, D., Interference in bacterial quorum sensing: a biopharmaceutical perspective, Front. Pharmacol., 2018, vol. 9, p. 203. https://doi.org/10.3389/fphar.2018.00203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ren, J.W., Liu, D., Tian, L., Wei, Y.Y., Proksch, P., Zeng, J.Z., and Lin, W.H., Venezuelines A-G, new phenoxazine-based alkaloids and aminophenols from Streptomyces venezuelae and the regulation of gene target Nur77, Bioorg. Med. Chem. Lett., 2013, vol. 23, pp. 301–304.

    Article  CAS  Google Scholar 

  20. Schmidt, R., Cordovez, V., de Boer, W., Raaijmakers, J., and Garbeva, P., Volatile affairs in microbial interactions, Int. Soc. Microb. Ecol., 2015, vol. 9, pp. 2329–2335.

    CAS  Google Scholar 

  21. Selvin, J., Shanmughapriya, S., Gandhimathi, R., Kiran, G.S., Ravji, T.R., Natarajaseenivasan, K., and Hema, T.A., Optimization and production of novel antimicrobial agents from sponge associated marine actinomycetes Nocardiopsis dassonvillei MAD08, Appl. Microbiol. Biotechnol., 2009, vol. 83, pp. 435–445.

    Article  CAS  Google Scholar 

  22. Stanbury, P., Whitaker, A., and Hall, S., Instrumentation and control, in Principles of Fermentation Technology, 3rd ed., Geraghty, F., Ed., Amsterdam: Butterworth-Heinemann, 2016, pp. 487–536.

    Google Scholar 

  23. Subramani, R. and Aalbersberg, W., Marine actinomycetes: an ongoning source of novel bioactive metabolites, Microbiol. Res., 2012, vol. 167, pp. 571–580.

    Article  CAS  Google Scholar 

  24. Subramani, R. and Aalbersberg, W., Culturable rare actinomycetes: diversity, isolation and marine natural product discovery, Appl. Microbiol. Biotechnol., 2013, vol. 97, pp. 9291–9321.

    Article  CAS  Google Scholar 

  25. Subramani, R. and Sipkema, D., Marine rare actinomycetes: a promising source of structurally diverse and unique novel natural products, Mar. Drugs, 2019, vol. 17, p. 249. https://doi.org/10.3390/md17050249

    Article  CAS  PubMed Central  Google Scholar 

  26. Ta, C.A., Freundorfer, M., Mah, T.F., Otarola-Rojas, M., Garcia, M., Sanchez-Vindas, P., Poveda, L., Maschek, J.A., Baker, B.J., Adonizio, A.L., Downum, K., Durst, T., and Arnason, J.T., Inhibition of bacterial quorum sensing and biofilm formation by extracts of neotropical rainforest plants, Planta Med., 2014, vol. 80, pp. 343–350.

    Article  CAS  Google Scholar 

  27. Ta, C.A.K. and Amason, J.T., Mini review of phytochemicals and plant taxa with activity as microbial biofilm and quorum sensing inhibitors, Molecules, 2016, vol. 21, p. 29.

    Article  Google Scholar 

  28. Teasdale, M.E., Donovan, K.A., Forschner-Dancause, S.R., and Rowley, D.C., Gram-positive marine bacteria as a potential resource for the discovery of quorum sensing inhibitors, Mar. Biotechnol., 2011, vol. 13, pp. 722–732.

    Article  CAS  Google Scholar 

  29. Wang, J.F., He, W.J., Qian, X.C., Wei, X.Y., Tian, X.P., Liao, L., Liao, S.R., Yang, B., Tu, Z.C., Chen, B., Wang, F.Z., Zhou, X.J., and Liu, Y.H., Three new indolyl diketopigerazine metabolites from arntarctic soil-derived fungus Penicillium sp. SCSIO 05705, RSC Adv., 2015, vol. 5, pp. 68736–68742.

    Article  CAS  Google Scholar 

  30. Wang, Y.J., Liu, L.L., Feng, Z.H., Liu, Z.Q., and Zheng, Y.G., Optimization of media composition and culture conditions for acarbose production by Actinoplanes utahensis ZJB-08196, World J. Microbiol. Biotechnol., 2011, vol. 27, pp. 2759–2766.

    Article  CAS  Google Scholar 

  31. Xiong, Y.H. and Liu, Y., Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling, Appl. Microbiol. Biotechnol., 2010, vol. 86, pp. 825–837.

    Article  CAS  Google Scholar 

  32. Yang, H.Y., Du, G., and Lu, K.F., Effect of bacteriostatic on the isolation of actinomycetes, Hubei Agricul. Sci., 2008, vol. 47, no. 4, pp. 435–437. https://doi.org/10.14088/j.cnki.issn0439-8114.2008.04.010

  33. Zhang, K., Yu, C., and Yang, S.T., Effects of soybean meal hydrolysate as the nitrogen source on seed culture morphology and fumaric acid production by Rhizopus oryzae, Process Biochem., 2015, vol. 50, pp. 173–179.

    Article  CAS  Google Scholar 

  34. Zou, G., Liao, X.J., Peng, Q., Chen, G.D., Wei, F.W., Xu, Z.X., Zhao, B.X., and Xu, S.H. A new α-pyrone from the deep-sea actinomycete Nocardiopsis dassonvillei subsp. dassonvillei DSM 43111(T), J. Asian Nat. Prod. Res., 2019, vol. 19, pp. 1232–1238.

    Article  Google Scholar 

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ACKNOWLEDGMENTS

The authors are grateful to Instrumental Analysis Center, Yangzhou University for the technique support in NMR and HRESI-MS measurement of pure compounds.

Funding

This study was generously supported by the open project of Key Laboratory of Marine Medicine, Guangdong Province and Key Laboratory of Tropical Marine Bio-Resources and Ecology, Chinese Academy of Sciences (2018011008).

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Authors and Affiliations

  1. College of Environmental Science and Engineering, Yangzhou University, 225009, Jiangsu, Yangzhou, China

    Li Miao, Sh. Qian, W. Jiang & K. Dong

  2. Key Laboratory of Tropical Marine Bio-Resources and Ecology, Chinese Academy of Sciences, 510301, Guangzhou, Guangdong Province, China

    Sh. Qi

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  1. Li Miao
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Correspondence to Li Miao.

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On behalf of all authors, the corresponding author states that there is no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Li Miao, Qian, S., Qi, S. et al. Culture Medium Optimization and Active Compounds Investigation of an Anti-Quorum Sensing Marine Actinobacterium Nocardiopsis dassonvillei JS106. Microbiology 90, 112–123 (2021). https://doi.org/10.1134/S0026261721010070

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