Abstract
The spoilage of aquatic products is mainly caused by the bacterial growth, and the specific spoilage organism (SSO) plays an important role. Quorum sensing (QS) is a microbial cell–cell communication system which is coordinated with the population density, and is controlled by N-acyl-homoserine lactone (AHLs) as the Gram-negative bacteria communication signals. In this study, the SSO was Pseudomonas fluorescens (PF-04), isolated from the turbot (Scophthalmus maximus L.) during aerobically refrigerated storage. The supernatant extract of PF-04 tested the AHLs activities utilizing biosensor Chromobacterium violaceum CV026. AHL production was influenced by the environment temperature, and AHL production reduced obviously at 10 °C compare with 25 °C. In Luria-Bertani (LB) supplemented with 0.5–1.0% NaCl, AHL production reached the maximum. The AHL production was also regulated by pH of culture medium, acidic condition was conducive to persistent existence of the AHL molecules, but the alkaline environment would cause chemically unstable of AHL molecules. QS system in P. flurosecens played an imperative role in biofilm formation, protease and siderophore production. AHLs could regulate above three factors in PF-04. In summary, this study showed that (1) the influence of different environmental conditions (temperature, NaCl and pH) on AHL production revealed the correlation of QS in foods and (2) that proved the effect of external AHLs to regulate the biofilm formation, protease and siderophore production in PF-04.
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References
Allesenholm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolkernielsen T (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59(4):1114–1128. https://doi.org/10.1111/j.1365-2958.2005.05008.x
Ams DA, Maurice PA, Hersman LE, Forsythe JH (2002) Siderophore production by an aerobic Pseudomonas mendocina bacterium in the presence of kaolinite. Chem Geol 188(3–4):161–170. https://doi.org/10.1111/j.1365-2958.2005.05008.x
Bahari S, Zeighami H, Mirshahabi H, Haghi F (2017) Inhibition of Pseudomonas aeruginosa quorum sensing by subinhibitory concentrations of curcumin with gentamicin and azithromycin. J Glob Antimicrob Re. https://doi.org/10.1016/S0009-2541(02)00077-3
Blana VA, Nychas GJ (2014) Presence of quorum sensing signal molecules in minced beef stored under various temperature and packaging conditions. Int J Food Microbiol 173(3):1. https://doi.org/10.1016/j.ijfoodmicro.2013.11.028
Brown AG, Luke RK (2010) Siderophore production and utilization by milk spoilage Pseudomonas species. J Dai Sci 93(4):1355–1363. https://doi.org/10.3168/jds.2009-2395
Bruhn JB, Christensen AB, Flodgaard LR, Nielsen KF, Larsen TO, Givskov M, Gram L (2004) Presence of acylated homoserine lactones (AHLs) and AHL-producing bacteria in meat and potential role of AHL in spoilage of meat. Appl Environ Microb 70(7):4293–4302. https://doi.org/10.1128/AEM.70.7.4293-4302.2004
Chen JW, Gan HM, Yin WF, Chan KG (2012) Genome sequence of Roseomonas sp. strain B5, a quorum-quenching N-acylhomoserine lactone-degrading bacterium isolated from Malaysian tropical soil. J Bacteriol 194(23):6681–6682. https://doi.org/10.1128/Jb.01866-12
Chen S, Jing X, Tang J, Fang Y, Zhou S (2017) Quorum sensing signals enhance the electrochemical activity and energy recovery of mixed-culture electroactive biofilms. Biosens Bioelectron 97(369–76):2017. https://doi.org/10.1016/j.bios.2017.06.024
Chong YM, Yin WF, Ho CY, Mustafa MR, Hadi AH, Awang K, Narrima P, Koh CL, Appleton DR, Chan KG (2016) Malabaricone C from Myristica cinnamomea exhibits anti-quorum sensing activity. J Nat Prod 74(10):2261–2264. https://doi.org/10.1021/np100872k
Christensen AB, Riedel K, Eberl L, Flodgaard LR, Molin S, Gram L, Givskov M (2003) Quorum-sensing-directed protein expression in Serratia proteamaculans B5a. Microbiology 149(2):471–483. https://doi.org/10.1099/mic.0.25575-0
Daniels R, Vanderleyden J, Michiels J (2004) Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28(3):261. https://doi.org/10.1016/j.femsre.2003.09.004
Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton J, Greenberg E (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280(5361):285–298. https://doi.org/10.1126/science.280.5361.295
Ferkinghoff-Borg J, Sams T (2014) Size of quorum sensing communities. Mol BioSys 10:103–109. https://doi.org/10.1039/c3mb70230h
Gram L (1993) Inhibitory effect against pathogenic and spoilage bacteria of Pseudomonas strains isolated from spoiled and fresh fish. Appl Environ Microb 59(7):2197–2203
Gram L (1996) The influence of substrate on siderophore production by fish spoilage bacteria. J Microbiol Meth 25(3):199–205. https://doi.org/10.1016/0167-7012(95)00079-8
Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M (2002) Food spoilage—interactions between food spoilage bacteria. Int J Food Microbiol 78:79–97. https://doi.org/10.1016/S0168-1605(02)00233-7
Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Ag 35(4):322–332. https://doi.org/10.1097/01.revmedmi.0000259645.20603.63
Juhas M, Eberl L, Tümmler B (2005) Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7(4):459. https://doi.org/10.1111/j.1462-2920.2005.00769.x
Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31(2):224. https://doi.org/10.1016/j.biotechadv.2012.10.004
Kim Y, Oh S, Park S, Seo JB, Kim SH (2008) Lactobacillus acidophilus reduces expression of enterohemorrhagic Escherichia coli O157:H7 virulence factors by inhibiting autoinducer-2-like activity. Food Control 19(11):1042–1050. https://doi.org/10.1016/j.foodcont.2007.10.014
Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286(2):885–886. https://doi.org/10.1038/286885a0
Li Ying Tan W-FY, Chan Kok-Gan (2012) Silencing quorum sensing through extracts of Melicope lunu-ankenda. Sensors 12(4):4339. https://doi.org/10.3390/s120404339
Liu M, Gray JM, Griffiths MW (2006) Occurrence of proteolytic activity and N-acyl-homoserine lactone signals in the spoilage of aerobically chill-stored proteinaceous raw foods. J Food Prot 69(11):2729–2737. https://doi.org/10.4315/0362-028X-69.11.2729
Loureiro V (2000) Spoilage yeasts in foods and beverages: characterisation and ecology for improved diagnosis and control. Food Res Int 33(3):247–256. https://doi.org/10.1016/S0963-9969(00)00044-2
Lund BM, Bairdparker TC, Gould GW (2000) Microbiological safety and quality of food. Springer, Berlin
Medinamartínez MS, Uyttendaele M, Meireman S, Debevere J (2007) Relevance of N-acyl-L-homoserine lactone production by Yersinia enterocolitica in fresh foods. J App Microbiol 102(4):1150–1158. https://doi.org/10.1016/S0963-9969(00)00044-2
Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104(1):313–322
Nychas GJE, Drosinos EH, Board RG (1998) Chemical changes in stored meat. In: Board R, Davies AR (eds) The microbiology of meat & poultry. Blackie Academic Professional, London, New York, pp 288–326
Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 14(9):576. https://doi.org/10.1038/nrmicro.2016.89
Pinto UM, Viana EDS, Martins ML, Vanetti MCD (2007) Detection of acylated homoserine lactones in gram-negative proteolytic psychrotrophic bacteria isolated from cooled raw milk. Food Control 18(10):1322–1327. https://doi.org/10.1016/j.foodcont.2006.09.005
Ragaert P, Devlieghere F, Debevere J (2007) Role of microbiological and physiological spoilage mechanisms during storage of minimally processed vegetables. Postharvest Biol Tec 44(3):185–194. https://doi.org/10.1016/j.postharvbio.2007.01.001
Rasch M, Andersen JB, Nielsen KF, Flodgaard LR, Christensen H, Givskov M, Gram L (2005) Involvement of bacterial quorum-sensing signals in spoilage of bean sprouts. App Environ Microb 71(6):3321–3330. https://doi.org/10.1128/AEM.71.6.3321-3330.2005
Reading N, Sperandio V (2006) Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254(1):1. https://doi.org/10.1111/j.1574-6968.2005.00001.x
Schuster M, Greenberg EP (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Me Microbiol 296(3):73–81. https://doi.org/10.1016/j.ijmm.2006.01.036
Shin SH, Lim Y, Lee SE, Yang NW, Rhee JH (2001) CAS agar diffusion assay for the measurement of siderophores in biological fluids. J Microbiol Methods 44:89–95. https://doi.org/10.1016/S0167-7012(00)00229-3
Solano C, Echeverz M, Lasa I (2014) Biofilm dispersion and quorum sensing. Curr Opin Microbiol 18(4):96. https://doi.org/10.1016/j.mib.2014.02.008
Vattem DA, Mihalik K, Crixell SH, Mclean RJ (2007) Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78(4):302–310. https://doi.org/10.1016/j.fitote.2007.03.009
Wang MZ, Zheng X, He HZ, Shen DS, Feng HJ (2012) Ecological roles and release patterns of acylated homoserine lactones in Pseudomonas sp. HF-1 and their implications in bacterial bioaugmentation. Bioresource Technol 125(338):119. https://doi.org/10.1016/j.biortech.2012.08.116
Wang HH, Ye KP, Zhang QQ, Dong Y, Xu XL, Zhou GH (2013) Biofilm formation of meat-borne Salmonella enterica and inhibition by the cell-free supernatant from Pseudomonas aeruginosa. Food Control 32(2):650–658. https://doi.org/10.1016/j.foodcont.2013.01.047
Wang T, Wei G, Qi H, Yang Y, Yan W, Sun B, Zhao T (2016) Quorum-sensing contributes to virulence, twitching motility, seed attachment and biofilm formation in the wild type strain Aac-5 of Acidovorax citrulli. Microb Pathogenesis 100:133–140. https://doi.org/10.1016/j.micpath.2016.08.039
Yarwood JM, Schlievert PM (2003) Quorum sensing in Staphylococcus infections. J Clin Invest 112(11):1620. https://doi.org/10.1172/JCI200320442
Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE, Goldner M, Dessaux Y, Cámara M, Smith H (2002) N-Acylhomoserine Lactones Undergo Lactonolysis in a pH-, Temperature-, and Acyl Chain Length-Dependent Manner during Growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70(10):5635–5646. https://doi.org/10.1128/IAI.70.10.5635-5646.2002
Zhu S, Wu H, Zeng M, Liu Z, Wang Y (2015) The involvement of bacterial quorum sensing in the spoilage of refrigerated Litopenaeus vannamei. Int J Food Microbiol 192(192):26. https://doi.org/10.1016/j.ijfoodmicro.2014.09.029
Zhu J, Zhao A, Feng L, Gao H (2016) Quorum sensing signals affect spoilage of refrigerated large yellow croaker (Pseudosciaena crocea) by Shewanella baltica. Int J Food Microbiol 217:146. https://doi.org/10.1016/10.1016/10.1016/j.ijfoodmicro.2015.10.020
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This work was financially supported by National Natural Science Foundation Projects (31471639, 31301572).
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Li, T., Yang, B., Li, X. et al. Quorum sensing system and influence on food spoilage in Pseudomonas fluorescens from turbot. J Food Sci Technol 55, 3016–3025 (2018). https://doi.org/10.1007/s13197-018-3222-y
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DOI: https://doi.org/10.1007/s13197-018-3222-y