Abstract
Shewanella baltica and Acinetobacter are among the predominant spoilage bacteria in refrigerated shrimp (Litopenaeus vannamei). S. baltica are incapable of producing acyl-homoserine lactone (AHL) quorum sensing signals, but can respond to environmental AHLs. In this paper, Acinetobacter was found to produce three AHLs, i.e. N-butanoyl-l-homoserine lactone (C4-HSL), N-(3-oxohexanoyl)-l-homoserine lactone (O-C6-HSL) and N-(3-oxooctanoyl)-l-homoserine lactone (O-C8-HSL), according to thin-layer chromatography using the bioreporter Agrobacterium tumefaciens A136. The agar diffusion and β-galactosidase assays revealed that S. baltica could eavesdrop on these three AHLs from Acinetobacter. Eavesdropping on Acinetobacter AHLs especially C4-HSL was found to boost the growth of S. baltica particularly under nutrient limiting conditions (up to 40-fold increase) in the co-culture experiments. The azocasein assay revealed that S. baltica produced fourfold more extracellular proteases in response to Acinetobacter AHLs. As demonstrated by the biofilm crystal violet staining assay and confocal laser scanning microscopy, eavesdropping also decreased the biofilm-forming capacity of Acinetobacter. By inoculation of S. baltica and Acinetobacter onto surface-sterilized shrimp, eavesdropping was found to endow a growth advantage to S. baltica in vivo, resulting in a 0.5 day shortened shelf life of shrimp according to total volatile basic nitrogen levels and sensory analysis. Overall, the AHL-dependent eavesdropping increased the spoilage potential of S. baltica, providing a fresh perspective on the spoilage process of refrigerated L. vannamei, and this may inspire the development of novel preservation techniques in the future to further reduce post-harvest loss of shrimp.
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References
Anbazhagan D, Mansor M, Yan GOS, Yusof MYM, Hassan H, Sekaran SD (2012) Detection of quorum sensing signal molecules and identification of an autoinducer synthase gene among biofilm forming clinical isolates of Acinetobacter spp. PLoS ONE 7:e36696
Atkinson S, Cámara M, Williams P (2007) N-acylhomoserine lactones, quorum sensing, and biofilm development in Gram-negative bacteria. In: Kjelleberg S, Givskov M (eds) The biofilm mode of life: mechanisms and adaptations. CRC Press, Boca Raton, pp 95–122
Bhargava N, Sharma P, Capalash N (2010) Quorum sensing in Acinetobacter: an emerging pathogen. Crit Rev Microbiol 36:349–360
Blana VA, Nychas GJE (2014) Presence of quorum sensing signal molecules in minced beef stored under various temperature and packaging conditions. Int J Food Microbiol 173:1–8
Botta JR, Lauder JT, Jewer MA (1984) Effect of methodology on total volatile basic nitrogen (TVB-N) determination as an index of quality of fresh Atlantic cod (Gadus morhua). J Food Sci 49:734–736
Bravo Z, Orruño M, Parada C, Kaberdin VR, Barcina I, Arana I (2016) The long-term survival of Acinetobacter baumannii, ATCC 19606 T, under nutrient-deprived conditions does not require the entry into the viable but non-culturable state. Arch Microbiol 198:1–9
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 149:471–483
Diggle SP, Griffin AS, Campbell GS, West SA (2007) Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411–414
Ercolini D, Russo F, Nasi A, Ferranti P, Villani F (2009) Mesophilic and psychrotrophic bacteria from meat and their spoilage potential in vitro and in beef. Appl Environ Microbiol 75:1990–2001
FAO (2017) Global aquaculture production 1950–2014. http://www.fao.org/fishery/statistics/global-aquaculture-production/query/en. Accessed 22 Feb 2017
Gonzalez RH, Nusblat A, Nudel BC (2001) Detection and characterization of quorum sensing signal molecules in Acinetobacter strains. Microbiol Res 155:271–277
Gu Q, Fu L, Wang Y, Lin J (2013) Identification and characterization of extracellular cyclic dipeptides as quorum-sensing signal molecules from Shewanella baltica, the specific spoilage organism of Pseudosciaena crocea during 4 °C storage. J Agric Food Chem 61:11645–11652
ISO (1989) Sensory analysis: general guidance for the design of test rooms. ISO 8589, Geneva
Ivnitsky H, Katz I, Minz D, Volvovic G, Shimoni E, Kesselman E, Dosoretz CG (2007) Bacterial community composition and structure of biofilms developing on nanofiltration membranes applied to wastewater treatment. Water Res 41:3924–3935
Kang YS, Park W (2010) Contribution of quorum-sensing system to hexadecane degradation and biofilm formation in Acinetobacter sp. strain DR1. J Appl Microbiol 109:1650–1659
Kawaguchi T, Chen YP, Norman RS, Decho AW (2008) Rapid screening of quorum-sensing signal N-acyl homoserine lactones by an in vitro cell-free assay. Appl Environ Microbiol 74:3667–3671
Li T, Cui F, Bai F, Zhao G, Li J (2016) Involvement of acylated homoserine lactones (AHLs) of Aeromonas sobria in spoilage of refrigerated turbot (Scophthalmus maximus L.). Sensors 16:1083
Macé S, Cardinal M, Jaffrès E, Cornet J, Lalanne V, Chevalier F, Sérot T, Pilet MF, Dousset X, Joffraud JJ (2014) Evaluation of the spoilage potential of bacteria isolated from spoiled cooked whole tropical shrimp (Penaeus vannamei) stored under modified atmosphere packaging. Food Microbiol 40:9–17
Miller E, Kjos M, Abrudan M, Robertsa IS, Veening JM, Rozena DE (2016) Crosstalk and eavesdropping among quorum sensing peptide signals that regulate bacteriocin production in Streptococcus pneumoniae. bioRxiv. https://doi.org/10.1101/087247
Morohoshi T, Ebata A, Nakazawa S, Kato N, Ikeda T (2005) N-acyl homoserine lactone-producing or-degrading bacteria isolated from the intestinal microbial flora of Ayu fish (Plecoglossus altivelis). Microbes Environ 20(4):264–268
Morohoshi T, Nakazawa S, Ebata A, Kato N, Ikeda T (2008) Identification and characterization of N-acylhomoserine lactone-acylase from the fish intestinal Shewanella sp. strain MIB015. Biosci Biotechnol Biochem 72:1887–1893
Moslehi-Jenabian S, Vogensen FK, Jespersen L (2011) The quorum sensing luxS gene is induced in Lactobacillus acidophilus NCFM in response to Listeria monocytogenes. Int J Food Microbiol 149(3):269–273
Okpala COR, Choo WS, Dykes GA (2014) Quality and shelf life assessment of Pacific white shrimp (Litopenaeus vannamei) freshly harvested and stored on ice. LWT Food Sci Technol 55:110–116
Ólafsdóttir G (2005) Volatile compounds as quality indicators in chilled fish: evaluation of microbial metabolites by an electronic nose. Ph.D. thesis, University of Iceland, IS
Olajuyigbe FM, Ajele JO (2008) Some properties of extracellular protease from Bacillus licheniformis LBBL-11 isolated from “iru”, a traditionally fermented African locust bean condiment. Afr J Biochem Res 2:206–210
Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in gram-negative bacteria. Nat Rev Microbiol 14:576–588
Qazi S, Middleton B, Muharram SH, Cockayne A, Hill P, O’Shea P, Chhabra SR, Cámara M, Williams P (2006) N-acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 74:910–919
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. Appl Environ Microbiol 71:3321–3330
Rawat S (2015) Food spoilage: microorganisms and their prevention. Asian J Plant Sci 5:47–56
Sarkar S, Chakraborty R (2008) Quorum sensing in metal tolerance of Acinetobacter junii BB1A is associated with biofilm production. FEMS Microbiol Lett 282:160–165
Skandamis PN, Nychas GJE (2012) Quorum sensing in the context of food microbiology. Appl Environ Microbiol 78:5473–5482
Stohr V, Joffraud JJ, Cardinal M, Leroi F (2001) Spoilage potential and sensory profile associated with bacteria isolated from cold-smoked salmon. Food Res Int 34:797–806
Svanevik CS, Roiha IS, Levsen A, Lunestad BT (2015) Microbiological assessment along the fish production chain of the Norwegian pelagic fisheries sector—results from a spot sampling programme. Food Microbiol 51:144–153
Venugopal V (1990) Extracellular proteases of contaminant bacteria in fish spoilage: a review. J Food Protect 53:341–350
Zhang C, Zhu S, Wu H, Jatt AN, Pan Y, Zeng M (2016) Quorum sensing involved in the spoilage process of the skin and flesh of vacuum-packaged farmed turbot (Scophthalmus maximus) stored at 4 °C. J Food Sci 81:M1–M9
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 192:26–33
Zhu S, Wu H, Zeng M, Zunying L, Zhao Dong S (2016) Regulation of spoilage-related activities of Shewanella putrefaciens and Shewanella baltica by an autoinducer-2 analogue, (z)-5-(bromomethylene)furan-2(5h)-one. J Food Process Preserv 39(6):719–728
Zhu S, Zhang C, Wu H, Jie J, Zeng M, Liu Z, Wang C, Yang H (2017) Spoilage of refrigerated (4 °C) Litopenaeus vannamei: cooperation between Shewanella species and contribution of cyclo-(L-Pro-L-Leu)-dependent quorum sensing. Int J Food Sci Technol 52(6):1517–1526
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This work was supported by the National Natural Science Foundation of China (Grant No. 31671919), the China Postdoctoral Science Foundation (Grant No. 2016M592252), and the Qingdao Postdoctoral Applied Research Project (Grant No. 2015239).
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Zhu, S., Wu, H., Zhang, C. et al. Spoilage of refrigerated Litopenaeus vannamei: eavesdropping on Acinetobacter acyl-homoserine lactones promotes the spoilage potential of Shewanella baltica. J Food Sci Technol 55, 1903–1912 (2018). https://doi.org/10.1007/s13197-018-3108-z
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DOI: https://doi.org/10.1007/s13197-018-3108-z