Inhibitory Activity of Tea Polyphenols on Biofilm Development of Shewanella putrefaciens

Journal of Food Processing and PreservationVolume 40, Issue 5 p. 910-917 Original Article Inhibitory Activity of Tea Polyphenols on Biofilm Development of Shewanella putrefaciens Fang Zhang, Fang Zhang College of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou, 310018 ChinaSearch for more papers by this authorJunli Zhu, Corresponding Author Junli Zhu [email protected] College of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou, 310018 ChinaCorresponding author. TEL/FAX: +86-571-88056656; EMAIL: [email protected]Search for more papers by this authorHuimin Wang, Huimin Wang College of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou, 310018 ChinaSearch for more papers by this author Fang Zhang, Fang Zhang College of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou, 310018 ChinaSearch for more papers by this authorJunli Zhu, Corresponding Author Junli Zhu [email protected] College of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou, 310018 ChinaCorresponding author. TEL/FAX: +86-571-88056656; EMAIL: [email protected]Search for more papers by this authorHuimin Wang, Huimin Wang College of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou, 310018 ChinaSearch for more papers by this author First published: 03 December 2015 https://doi.org/10.1111/jfpp.12669Citations: 8Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Shewanella putrefaciens has been identified as the main specific spoilage organism during iced storage of marine fish. In this study, the inhibitory effects of tea polyphenol (TP) against biofilms of Sh. putrefaciens were evaluated. The addition of TP at the initial time exhibited the strongest biofilm inhibitory effect, while applying after 10 h or later did not show significant inhibitory effect. TP significantly inhibited the initial cell attachment on stainless steel in a concentration-dependent manner. Subsequently, the biofilm mature curve and metabolic activity decreased considerably after incubation with subminimal inhibitory concentration of TP. Scanning electron micrographs confirmed visual disruption in a number of extracellular polymeric substances and alteration in dimensional structure of Sh. putrefaciens. Our results indicated that Sh. putrefaciens biofilms were susceptible to TP, suggesting its potential in controlling bacterial biofilms in food processing. Practical Applications Our findings provide evidence for the potential application of tea polyphenols in prolonging the shelf life of marine fish by inhibiting the biofilm development of Shewanella putrefaciens. References Almajano, M.P., Rosa, C.J., Angel, L.J.Z. and Michael, H.G. 2008. Antioxidant and antimicrobial activities of tea infusions. Food Chem. 108, 55–63. Anna, R.B., La Simona, T.M., Gioia, B., Spiridione, G., Vincenzo, E. and Dario, R. 2003. (-)Epigallocatechin-3-gallate inhibits gelatinase activity of some bacterial isolates from ocular infection, and limits their invasion through gelatine. Biochim. Biophys. Acta. 1620, 273–281. Bagge, D., Hjelm, M., Johansen, C., Huber, I. and Gram, L. 2001. Shewanella putrefaciens adhesion and biofilm formation on food processing surfaces. Appl. Environ. Microbiol. 67, 2319–2325. Blanco, A.R., Sudano-Roccaro, A., Spoto, G.C., Nostro, A. and Rusciano, D. 2005. Epigallocatechin gallate inhibits biofilm formation by ocular Staphylococcal isolates. Antimicrob. Agents Chemother. 49, 4339–4343. Carson, C.F., Mee, B.J. and Riley, T.V. 2002. Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrob. Agents Chemother. 46, 1914–1920. Cooper, R., Morre, D.J. and Morre, D.M. 2005. Medicinal benefits of green tea: Part I. Review of noncancer health benefits. J. Altern. Complement. Med. 11, 521–528. Costerton, J.W., Stewart, P.S. and Greenberg, E.P. 1999. Bacterial biofilms: A common cause of persistent infections. Science 284, 1318–1322. Djordjevic, D., Wiedmann, M. and McLandsborough, L.A. 2002. Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl. Environ. Microbiol. 68, 2950–2958. Donlan, R.M. 2002. Biofilms: Microbial life on surfaces. Emerg. Infect. Dis. 8, 881–890. Evensen, N.A. and Braun, P.C. 2009. The effects of tea polyphenols on Candida albicans: Inhibition of biofilm formation and proteasome inactivation. Can. J. Microbiol. 55, 1033–1039. Gunduz, G. and Tuncel, G. 2006. Biofilm formation in an ice cream plant. Antonie Van Leeuwenhoek 89, 329–336. Hamilton-Miller, J.M. 1995. Antimicrobial properties of tea (Camellia sinensis L. Antimicrob. Agents Chemother. 39, 2375–2377. Jadhav, S., Shah, R., Bhave, M. and Palombo, E.A. 2013. Inhibitory activity of yarrow essential oil on Listeria planktonic cells and biofilms. Food Control. 29, 125–130. Kim, J.E., Choi, N.H. and Kang, S.C. 2007. Anti-listerial properties of garlic shoot juice at growth and morphology of Listeria monocytogenes. Food Control. 18, 1198–1203. Kohda, C., Yanagawa, Y. and Shimamura, T. 2008. Epigallocatechin gallate inhibits intracellular survival of Listeria monocytogenes in macrophages. Biochem. Biophys. Res. Commun. 365, 310–315. Kubota, H., Senda, S., Tokuda, H., Uchiyama, H. and Nomura, N. 2009. Stress resistance of biofilm and planktonic Lactobacillus plantarum subsp. plantarum JCM 1149. Food Microbiol. 26, 592–597. Lee, J.H., Kim, Y.G., Cho, H.S., Ryu, S.Y., Cho, M.H. and Lee, J. 2014. Coumarins reduce biofilm formation and the virulence of Escherichia coli O157:H7. Phytomedicine 21, 1037–1042. Lindsay, D. and von Holy, A. 1997. Evaluation of dislodging methods for laboratory grown bacterial biofilms. Food Microbiol. 14, 383–390. Mah, T.C. and O'Toole, G.A. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9, 34–39. Nakane, H. and Ono, K. 1990. Differential inhibitory effects of some catechin derivatives on the activities of human immunodeficiency virus reverse transcriptase and alular deoxyribonudeic and ribonucleic acid polymerases. Biochemistry 29, 2841–2845. Nam, S., Smith, D.M. and Dou, Q.P. 2001. Ester bond-containing tea polyphenols potently inhibit proteasome activity in vitro and in vivo. J. Biol. Chem. 276, 13322–13330. Obuekwe, C.O., Westlake, D.W.S., Cook, F.D. and William, C.J. 1981. Surface changes in mild steel coupons from the action of corrosion-causing bacteria. Appl. Environ. Microbiol. 41, 766–774. Packiavathy, I.A.S.V., Agilandeswari, P., Musthafa, K.S., Pandian, S.K. and Ravi, A.V. 2012. Antibiofilm and quorum sensing inhibitory potential of Cuminum cyminum and its secondary metabolite methyl eugenol against Gram negative bacterial pathogens. Food Res. Int. 45, 85–92. Packiavathy, I.A.S.V., Priya, S., Pandian, S.K. and Ravi, A.V. 2014. Inhibition of biofilm development of uropathogens by curcumin – An anti-quorum sensing agent from Curcuma longa Coumarins. Food Chem. 148, 453–460. Percival, R.S., Devine, D.A., Duggal, M.S., Chartron, S. and Marsh, P.D. 2006. The effect of cocoa polyphenols on the growth, metabolism, and biofilm formation by Streptococcus mutans and Streptococcus sanguinis. Eur. J. Oral Sci. 114, 343–348. Pettit, R.K., Weber, C.A., Kean, M.J., Hoffman, H., Pettit, G.R., Tan, R., Franks, K.S. and Horton, M.L. 2005. Microplate alamar blue assay for Staphylococcus epidermis biofilm susceptibility testing. Antimicrob. Agents Chemother. 49, 2612–2617. Priha, O., Virkajarvi, V., Juvonen, R., Puupponen-Pimia, R., Nohynek, L., Alakurtti, S., Pirttimaa, M. and Storgards, E. 2014. Quorum sensing signalling and biofilm formation of brewery-derived bacteria, and inhibition of signalling by natural compounds. Curr. Microbiol. 69, 617–627. Sandasi, M., Leonard, C.M. and Viljoen, A.M. 2008. The effect of five common essential oil components on Listeria monocytogenes biofilms. Food Control. 19, 1070–1075. Sandasi, M., Leonard, C.M. and Viljoen, A.M. 2010. The in vitro antibiofilm activity of selected culinary herbs and medicinal plants against Listeria monocytogenes. Lett. Appl. Microbiol. 50, 30–35. Shafreena, R.M.B., Selvarajb, C., Singhb, S.K. and Pandiana, S.K. 2014. In silico and in vitro studies of cinnamaldehyde and their derivatives against LuxS in Streptococcus pyogenes: Effects on biofilm and virulence genes. J. Mol. Recognit. 27, 106–116. Silván, J.M., Mingo, E., Hidalgo, M., De Pascual-Teresa, S., Carrascosa, A.V. and Martinez-Rodriguez, A.J. 2013. Antibacterial activity of a grape seed extract and its fractions against Campylobacter spp. Food Control. 29, 25–31. Sinde, E. and Carballo, J. 2000. Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluoroethylene: The influence of free energy and the effect of commercial sanitizers. Food Microbiol. 17, 439–447. Vogel, B.F., Venkateswaran, K., Satomi, M. and Gram, L. 2005. Identification of Shewanella baltica as the most important H2S-producing species during iced cold storage of Danish marine fish. Appl. Environ. Microbiol. 71, 6689–6697. Yi, L., Wang, Y., Ma, Z., Zhang, H., Li, Y., Zheng, J.X., Yang, Y.C., Fan, H.J. and Lu, C.P. 2014. Biofilm formation of Streptococcus equi ssp. zooepidemicus and comparative proteomic analysis of biofilm and planktonic cells. Curr. Microbiol. 69, 227–233. Yi, S.M., Zhu, J.L., Fu, L.L. and Li, J.R. 2010. Tea polyphenols inhibit Pseudomonas aeruginosa through damage to the cell membrane. Int. J. Food Microbiol. 144, 111–117. Zhang, J.M., Rui, X., Wang, L., Guan, Y., Sun, X.M. and Dong, M.S. 2014. Polyphenolic extract from Rosa rugosa tea inhibits bacterial quorum sensing and biofilm formation. Food Control. 42, 125–131. Citing Literature Volume40, Issue5October 2016Pages 910-917 ReferencesRelatedInformation