Novel Perspectives on the Quorum Sensing Inhibitors (QSIs)/Quorum Quenchers (QQs) in Food Preservation and Spoilage

  • Saqib Hassan
  • Tanveer Ahmad
  • Mudasir Bashir
  • G. Seghal Kiran
  • Joseph SelvinEmail author


Quorum sensing (QS) regulates major bacterial behaviors such as virulence, antibiotic resistance biofilm formation, and bioluminescence when the population reaches high density. The role of QS in biofilm formation and virulence is an extreme problem for food safety, biofilm-related infectious diseases, etc. Food spoilage is a consequence of degrading enzymatic activities, viz., proteolytic, lipolytic, chitinolytic, and pectinolytic, of some food-associated bacteria. Several activities associated with the deterioration of goods are regulated by QS, suggesting a potential role of such cell-to-cell communication in food spoilage. Therefore, interrupting QS mechanism might be an alternative strategy to develop novel QS-based antibacterial/anti-biofilm drugs. QS-based antibacterial/anti-biofilm agents can be used to manage foodborne pathogens and biofilm formation in food industries. Efforts to disrupt biofilms have enabled the identification of bioactive molecules produced by prokaryotes and eukaryotes. Production and bioactivity of mushroom polysaccharide was enhanced by using microbial QS molecules. Plant food extracts and phytochemicals were found to have anti-QS properties. Organic acids can act as effective potential sanitizers in reducing microbial load associated with fresh fruits and vegetables. Moreover, organic acids are known to be used as food preservatives due to their antimicrobial potential. Most approaches to use QQ as an anti-virulence strategy are still in initial phase; the increasing number of organisms and enzymes known to interfere with QS opens new perspectives for the development of innovative antibacterial strategies to prevent food spoilage.


Quorum Enzymes Food Biofilms Pathogenicity 


  1. Adam B, Baillie GS, Douglas LJ (2002) Mixed-species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 51:344–349CrossRefGoogle Scholar
  2. Agle ME (2003) Shigella boydii 18: characterization and biofilm formation [PhD thesis]. University of Illinois, UrbanaGoogle Scholar
  3. Ahmer BMM (2004) Cell-to-cell signaling in Escherichia coli and Salmonella enterica. Mol Microbiol 52:933–945CrossRefGoogle Scholar
  4. Alavi HED, Hansen LT (2013) Kinetics of biofilm formation and desiccation survival of Listeria monocytogenes in single and dual species biofilms with Pseudomonas fluorescens, Serratia proteamaculans or Shewanella baltica on food-grade stainless steel surfaces. Biofouling 29(10):1253–1268CrossRefGoogle Scholar
  5. Almasoud A, Hettiarachchy N, Rayaprolu S, Babu D, Kwon YM, Mauromoustakos A (2016) Inhibitory effects of lactic and malic organic acids on autoinducer type 2 (AI-2) QS of Escherichia coli O157: H7 and Salmonella typhimurium. LWT-Food Sci Technol 66:560–564CrossRefGoogle Scholar
  6. Almeida C, Azevedo NF, Santos S, Keevil CW, Vieira MJ (2011) Discriminating multi-species populations in biofilms with peptide nucleic acid fluorescence in situ hybridization (PNA FISH). PLoS One 6(3):e14786PubMedCentralCrossRefPubMedGoogle Scholar
  7. Ammor MS, Michaelidis C, Nychas GJE (2008) Insights into the role of quorum sensing in food spoilage. J Food Prot 71(7):1510–1525PubMedCentralCrossRefPubMedGoogle Scholar
  8. Amrutha B, Sundar K, Shetty PH (2017) Effect of organic acids on biofilm formation and quorum signaling of pathogens from fresh fruits and vegetables. Microb Pathog 111:156–162CrossRefGoogle Scholar
  9. Annous BA, Sapers GM, Mattrazzo AM, Riordan DCR (2001) Efficacy of washing with a commercial flatbed brush washer, using conventional and experimental washing agents, in reducing populations of Escherichia coli on artificially inoculated apples. J Food Prot 64:159–163CrossRefGoogle Scholar
  10. Annous BA, Burke A, Sites JE (2004) Surface pasteurization of whole fresh cantaloupes inoculated with Salmonella Poona or Escherichia coli. J Food Prot 67:1876–1885CrossRefGoogle Scholar
  11. Annous BA, Sapers GM, Jones DM, Burke A (2005) Improved recovery procedure for evaluation of sanitizer efficacy in disinfecting contaminated cantaloupes. J Food Sci 70:M242–M247CrossRefGoogle Scholar
  12. Annous BA, Fratamico PM, Smith JL (2009) Quorum sensing in biofilms: why bacteria behave the way they do. J Food Sci 74(1):R1–R14CrossRefGoogle Scholar
  13. Atkinson S, Chang C-Y, Sockett RE, Cámara M, Williams P (2006) QS in Yersinia enterocolitica controls swimming and swarming motility. J Bacteriol 188:1451–1461PubMedCentralCrossRefPubMedGoogle Scholar
  14. Bagge D, Metthe H, Charlotte J, Ingrid H, Lone G (2001) Shewanella putrefaciens adhesion and biofilm formation on food processing surfaces. Appl Environ Microbiol 67(5):2319–2325PubMedCentralCrossRefPubMedGoogle Scholar
  15. Bandara HMHN, Yau JYY, Watt RM, Jin LJ, Samaranayake LP (2010) Peudomonas aeruginosa inhibits in-vitro Candida biofilm development. BMC Microbiol 10:125PubMedCentralCrossRefPubMedGoogle Scholar
  16. Bassler BL, Wright M, Showalter RE, Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9(4):773–786CrossRefGoogle Scholar
  17. Bassler BL, Wright M, Silverman MR (1994) Sequence and function of LuxO, a negative regulator of luminescence in Vibrio harveyi. Mol Microbiol 12(3):403–412CrossRefGoogle Scholar
  18. Behnke S, Camper AK (2012) Chlorine dioxide disinfection of single and dual species biofilms, detached biofilm and planktonic populations. Biofouling 28(6):635–647CrossRefGoogle Scholar
  19. Blana VA, Nychas GJE (2014) Presence of QS signal molecules in minced beef stored under various temperature and packaging conditions. Int J Food Microbiol 173:1–8CrossRefGoogle Scholar
  20. Boddy L, Wimpenny JW (1992) Ecological concepts in food microbiology. Soc Appl Bacteriol Symp Ser 21:23S–38SGoogle Scholar
  21. Brandl MT, Carter MQ, Parker CT, Chapman MR, Huynh S, Zhou Y (2011) Salmonella biofilm formation on Aspergillus niger involves cellulose–chitin interactions. PLoS One 6(10):e25553PubMedCentralCrossRefPubMedGoogle Scholar
  22. Bridier A, Sanchez-Vizuete M del P, Le Coq D, Aymerich S, Meylheuc T, Maillard JY, Thomas V, Dubois-Brissonnet F, Briandet R (2012) Biofilms of a Bacillus subtilis hospital isolate protect Staphylococcus aureus from biocide action. PLoS One 7(9):e44506PubMedCentralCrossRefPubMedGoogle Scholar
  23. 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 Microbiol 70:4293–4302PubMedCentralCrossRefPubMedGoogle Scholar
  24. Burmølle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923PubMedCentralCrossRefPubMedGoogle Scholar
  25. Byers JT, Lucas C, Salmond GPC, Welch M (2002) Nonenzymatic turnover of an Erwinia carotovora quorum-sensing signaling molecule. J Bacteriol 184:1163–1171PubMedCentralCrossRefPubMedGoogle Scholar
  26. Carpentier B, Chassaing D (2004) Interactions in biofilms between Listeria monocytogenes and resident microorganisms from food industry premises. Intl J Food Microbiol 97(2):111–122CrossRefGoogle Scholar
  27. Castonguay MH, van der Schaaf S, Koester W, Krooneman J, van der Meer W, Harmsen H, Landini P (2006) Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Res Microbiol 157(5):471–478CrossRefGoogle Scholar
  28. CDC National (2012) Center for Emerging and Zoonotic Infectious Diseases. Retrieved on 2 OctoberGoogle Scholar
  29. Cerqueira L, Oliveira JA, Nicolau A, Azevedo NF, Vieira MJ (2013) Biofilm formation with mixed-species of Pseudomonas aeruginosa/Escherichia coli on silicone using artificial urine to mimic urinary catheters. Biofouling 29(7):829–840CrossRefGoogle Scholar
  30. Chai Y, Tsai CS, Cho H, Winanas SC (2007) Reconstitution of the biochemical activities of the AttJ repressor and the AttK, Atl and AttM catabolic enzymes of Agrobacterium tumefaciens. J Bacteriol 2(189):3674–3679PubMedCentralCrossRefPubMedGoogle Scholar
  31. Challan Belval S, Gal L, Margiewes S, Garmyn D, Piveteau P, Guzzo J (2006) Assessment of the roles of LuxS, S-ribosyl homocysteine, and autoinducer 2 in cell attachment during biofilm formation by Listeria monocytogenes EGD-e. Appl Environ Microbiol 72:2644–2650PubMedCentralCrossRefPubMedGoogle Scholar
  32. Chorianopoulos NG, Giaouris ED, Skandamis PN, Haroutounian SA, Nychas GJE (2008) Disinfectant test against monospecies and mixed-species biofilms composed of technological, spoilage and pathogenic bacteria: bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid–base sanitizers. J Appl Microbiol 104:1586–1596CrossRefGoogle Scholar
  33. Chorianopoulos NG, Giaouris ED, Kourkoutas Y, Nychas GJE (2010) Inhibition of the early stage of Salmonella enterica serovar Enteritidis biofilm development on stainless steel by cell-free supernatant of a Hafnia alvei culture. Appl Environ Microbiol 76(6):2018–2022PubMedCentralCrossRefPubMedGoogle Scholar
  34. 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 149:471–483CrossRefGoogle Scholar
  35. Cloak OM, Solow BT, Briggs CE, Chen C-Y, Fratamico PM (2002) QS and production of autoinducer-2 in Campylobacter spp., Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in foods. Appl Environ Microbiol 68:4666–4671PubMedCentralCrossRefPubMedGoogle Scholar
  36. Cole SP, Harwood J, Lee R, She R, Guiney DG (2004) Characterization of monospecies biofilm formation by Helicobacter pylori. J Bacteriol 186:3124–3132PubMedCentralCrossRefPubMedGoogle Scholar
  37. Cowan SE, Gilbert E, Liepmann D, Keasling JD (2000) Commensal interactions in a dual-species biofilm exposed to mixed organic compounds. Appl Environ Microbiol 66(10):4481–4485PubMedCentralCrossRefPubMedGoogle Scholar
  38. Da Re S, Valle J, Charbonnel N, Beloin C, Latour-Lambert P, Faure P, Turlin E, Le Bougu’enec C, Renauld-Mong’enie G, Forestier C, Ghigo JM (2013) Identification of commensal Escherichia coli genes involved in biofilm resistance to pathogen colonization. PLoS One 8(5):e61628PubMedCentralCrossRefPubMedGoogle Scholar
  39. Dalgaard P (1995) Qualitative and quantitative characterization of spoilage bacteria from packed fish. Int J Food Microbiol 26(3):319CrossRefGoogle Scholar
  40. Dalgaard P, Mejlholm O, Christiansen TJ, Huss HH (1997) Importance of Photobacterium phosphoreum in relation to spoilage of modified-atmosphere–packed fish products. Lett Appl Microbiol 24:373–378CrossRefGoogle Scholar
  41. Defoirdt T, Crab R, Woods TK, Sorgeloos P, Verstraete W, Bossier P (2006) Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbellii and Vibrio parahaemolyticus isolates. Appl Environ Microbiol 72:6419–6423PubMedCentralCrossRefPubMedGoogle Scholar
  42. DeWaal CS, Barlow K (2002) Outbreak alert! Closing the gaps in our federal food safety net, 5th edn. Center for Science in the Public Interest, Washington, DCGoogle Scholar
  43. Ding T, Li T, Wang Z, Li J (2017) Curcumin liposomes interfere with QS system of Aeromonas sobria and in silico analysis. Sci Rep 7(1):8612PubMedCentralCrossRefPubMedGoogle Scholar
  44. do Valle Gomes MZ, Nitschke M (2012) Evaluation of rhamnolipid and surfactin to reduce the adhesion and remove biofilms of individual and mixed cultures of food pathogenic bacteria. Food Control 25(2):441–447CrossRefGoogle Scholar
  45. Dogan B, Boor KJ (2003) Genetic diversity and spoilage potentials among Pseudomonas spp. isolated from fluid milk products and dairy processing plants. Appl Environ Microbiol 69:130–138PubMedCentralCrossRefPubMedGoogle Scholar
  46. Dong YH, Zhang LH (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43(special issue #S):101–109Google Scholar
  47. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890PubMedCentralCrossRefPubMedGoogle Scholar
  48. Esteves CL, Jones BD, Clegg S (2005) Biofilm formation by Salmonella enterica serovar Typhimurium and Escherichia coli on epithelial cells following mixed inoculations. Infect Immun 73(8):5198–5203PubMedCentralCrossRefPubMedGoogle Scholar
  49. Faille C, Jullien C, Fontaine F, Bellon-Fontaine M-N, Slomianny C, Benezech T (2002) Adhesion of Bacillus spores and Escherichia coli cells to inert surfaces: role of surface hydrophobicity. Can J Microbiol 48:728–738CrossRefGoogle Scholar
  50. Flodgaard LR, Dalgaard P, Andersen JB, Nielsen KF, Givskov M, Gram L (2005) Nonbioluminescent strains of Photobacterium phosphoreum produce the cell-to-cell communicationsignal N-(3-hydroxyoctanoyl) homoserine lactone. Appl Environ Microbiol 71:2113–2120PubMedCentralCrossRefPubMedGoogle Scholar
  51. Fu L, Wang C, Liu N, Ma A, Wang Y (2018) QS system-regulated genes affect the spoilage potential of Shewanella baltica. Food Res Int 107:1–9CrossRefGoogle Scholar
  52. Fuqua WC, Winans SC, Greenberg EP (1994 Jan) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176(2):269PubMedCentralCrossRefPubMedGoogle Scholar
  53. Giaouris E, Chorianopoulos N, Doulgeraki A, Nychas GJ (2013) Co-culture with Listeria monocytogenes within a dual-species biofilm community strongly increases resistance of Pseudomonas putida to benzalkonium chloride. PLoS One 8(10):e77276PubMedCentralCrossRefPubMedGoogle Scholar
  54. Givskov M, de Nys R, Manefield M, Gram L, Maximilien RIA, Eberl LEO et al (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178(22):6618–6622PubMedCentralCrossRefPubMedGoogle Scholar
  55. Gori K, Moslehi-Jenabian S, Purrotti M, Jespersen L (2012) Autoinducer-2 activity produced by bacteria found in smear of surface ripened cheeses. Int Dairy J 21:48–53CrossRefGoogle Scholar
  56. Gram L, Huss HH (1996 Nov 1) Microbiological spoilage of fish and fish products. Int J Food Microbiol 33(1):121–137CrossRefGoogle Scholar
  57. Gram L, Melchiorsen J, Spanggaard B, Huber I, Nielsen TF (1999) Inhibition of Vibrio anguillarum byPseudomonas fluorescens AH2, a possible probiotic treatment of fish. Appl Environ Microbiol 65(3):969–973Google Scholar
  58. Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M (2002) Food spoilage—interactions between food spoilage bacteria. Int J Food Microbiol 78:79–97CrossRefGoogle Scholar
  59. Gross M, Cramton SE, Götz F, Peschel A (2001) Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun 69:3423–3426PubMedCentralCrossRefPubMedGoogle Scholar
  60. Guillier L, Stahl V, Hezard B, Notz E, Briandet R (2008) Modelling the competitive growth between Listeria monocytogenes and biofilm microflora of smear cheese wooden shelves. Intl J Food Microbiol 128(1):51–57CrossRefGoogle Scholar
  61. Habimana O, Møretrø T, Langsrud SS, Lene K, Vestby LK, Live L, Nesse LL, Heir E (2010a) Micro ecosystems from feed industry surfaces: a survival and biofilm study of Salmonella versus host resident flora strains. BMC Vet Res 6:48PubMedCentralCrossRefPubMedGoogle Scholar
  62. Habimana O, Heir E, Langsrud S, Asli AW, Møretrø T (2010b) Enhanced surface colonization by Escherichia coli O157:H7 in biofilms formed by an Acinetobacter calcoaceticus isolate from meat-processing environments. Appl Environ Microbiol 76(13):4557–4559PubMedCentralCrossRefPubMedGoogle Scholar
  63. Hammer BK, Bassler BL (2003) QS controls biofilm formation in Vibrio cholerae. Mol Microbiol 50:101–114CrossRefGoogle Scholar
  64. Henke JM, Bassler BL (2004) QS regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186:3794–3805PubMedCentralCrossRefPubMedGoogle Scholar
  65. Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112(9):1300–1307PubMedCentralCrossRefPubMedGoogle Scholar
  66. Huis in’t Veld JHJ (1996) Microbial and biochemical spoilage of foods: an overview. Int J Food Microbiol 33:1–18CrossRefGoogle Scholar
  67. Ibusquiza PS, Herrera JJ, V’azquez-S’anchez D, Cabo ML (2012) Adherence kinetics, resistance to benzalkonium chloride and microscopic analysis of mixed-species biofilms formed by Listeria monocytogenes and Pseudomonas putida. Food Control 25:202–210CrossRefGoogle Scholar
  68. Ica T, Caner V, Istanbullu O, Nguyen HD, Ahmed B, Call DR, Beyenal H (2012) Characterization of mono and mixed-species Campylobacter jejuni biofilms. Appl Environ Microbiol 78(4):1033–1038PubMedCentralCrossRefPubMedGoogle Scholar
  69. Jagmann N, von Rekowski KS, Philipp B (2012) Interactions of bacteria with different mechanisms for chitin degradation result in the formation of a mixed-species biofilm. FEMS Microbiol Lett 326(1):69–75CrossRefGoogle Scholar
  70. Jahid IK, Ha SD (2012) A review of microbial biofilms of produce: future challenge to food safety. Food Sci Biotechnol 21(2):299–316CrossRefGoogle Scholar
  71. Jahid IK, Ha SD (2014) The paradox of mixed-species biofilms in the context of food safety. Compr Rev Food Sci Food Saf 13(5):990–1011CrossRefGoogle Scholar
  72. Jahid IK, Han N, Srey S, Ha SD (2014) Competitive interactions inside mixed-species biofilms of Salmonella typhimurium and cultivable indigenous microorganisms on lettuce enhance microbial resistance of their sessile cells to ultraviolet C (UV-C) irradiation. Food Res Int 55:445–454CrossRefGoogle Scholar
  73. Jarrett CO, Deak E, Isherwood KE, Oyston PC, Fisher ER, Whitney AR, Kobayashi SD, DeLeo FR, Hinnebusch BJ (2004) Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J Infect Dis 190:783–792CrossRefGoogle Scholar
  74. Jay JM, Vilai JP, Hughes ME (2003) Profile and activity of the bacterial biota of ground beef held from freshness to spoilage at 5–7 °C. Int J Food Microbiol 81:105–111CrossRefGoogle Scholar
  75. Jeon B, Itoh K, Ryu S (2005) Promoter analysis of cytolethal distending toxin genes (cdtA, B and C) and effect of a luxS mutation on CDT production in Campylobacter jejuni. Microbiol Immunol 49:599–603CrossRefGoogle Scholar
  76. Johnson MR et al (2005) Population density-dependent regulation of exopolysaccharide formation in the hyperthermophilic bacterium Thermotoga maritima. Mol Microbiol 55:664–674PubMedCentralCrossRefPubMedGoogle Scholar
  77. Jorgensen LV, Huss HH, Dalgaard P (2000) The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J Appl Microbiol 89:920–934CrossRefGoogle Scholar
  78. Joshua GWP, Karlyshev AV, Smith MP, Isherwood KE, Titball RW, Wren BW (2003) A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology 149:3221–3229CrossRefGoogle Scholar
  79. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31(2):224–245PubMedCentralCrossRefPubMedGoogle Scholar
  80. Kawarai T, Furukawa S, Ogihara H, Yamasaki M (2007) Mixed-species biofilm formation by lactic acid bacteria and rice wine yeasts. Appl Environ Microbiol 73:4673–4676PubMedCentralCrossRefPubMedGoogle Scholar
  81. Kay MK, Erwin TC, McLean RJ, Aron GM (2011) Bacteriophage ecology in Escherichia coli and Pseudomonas aeruginosa mixed-biofilm communities. Appl Environ Microbiol 77(3):821–829CrossRefGoogle Scholar
  82. Kiran GS, Hassan S, Sajayan A, Selvin J (2017) Quorum quenching compounds from natural sources. In: Bioresources and bioprocess in biotechnology. Springer, Singapore, pp 351–364CrossRefGoogle Scholar
  83. Kirwan JP, Gould TA, Schweizer HP, Bearden SW, Murphy RC, Churchill MEA (2006) Quorum-sensing signal synthesis by the Yersinia pestis acyl-homoserine lactone synthase YspI. J Bacteriol 188:784–788PubMedCentralCrossRefPubMedGoogle Scholar
  84. Kostaki M, Chorianopoulos N, Braxou E, Nychas GJ, Giaouris E (2012) Differential biofilm formation and chemical disinfection resistance of sessile cells of Listeria monocytogenes strains under monospecies and dual-species (with Salmonella enterica) conditions. Appl Environ Microbiol 78(8):2586–2595PubMedCentralCrossRefPubMedGoogle Scholar
  85. Koutsoumanis K, Nychas G-JE (1999) Chemical and sensory changes associated with microbial flora of Mediterranean boque (Boops boops) stored aerobically at 0, 3, 7, and 10°C. Appl Environ Microbiol 65:698–706PubMedCentralPubMedGoogle Scholar
  86. Kuznetsova MV, Maslennikova IL, Karpunina TI, Nesterova LY, Demakov VA (2013) Interactions of Pseudomonas aeruginosa in predominant biofilm or planktonic forms of existence in mixed-species with Escherichia coli in vitro. Can J Microbiol 59(9):604–610CrossRefGoogle Scholar
  87. Lade H, Paul D, Kweon JH (2014) Quorum quenching mediated approaches for control of membrane biofouling. Int J Biol Sci 10(5):550PubMedCentralCrossRefPubMedGoogle Scholar
  88. Lau YY, Sulaimane J, Chen JW, Yin WF, Chan KG (2013) Quorum sensing activity of Enterobacter asburiae isolated from lettuce leaves. Sensors 13:14189–14199CrossRefGoogle Scholar
  89. Lazazzera BA, Grossman AD (1998 Jul 1) The ins and outs of peptide signaling. Trends Microbiol 6(7):288–294PubMedCentralCrossRefPubMedGoogle Scholar
  90. Lebert I, Leroy S, Talon R (2007) Effect of industrial and natural biocides on spoilage, pathogenic and technological strains grown in biofilm. Food Microbiol 24(3):281–287CrossRefGoogle Scholar
  91. Lee JH, Cho HS, Joo SW, Regmi SC, Kim JA, Ryu CM, Ryu SY, Cho MH, Lee J (2013a) Diverse plant extracts and trans-resveratrol inhibit biofilm formation and swarming of Escherichia coli O157:H7. Biofouling 29(10):1189–1203CrossRefGoogle Scholar
  92. Lee KW, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA (2013b) Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 8. Scholar
  93. Liao CH (2007) Inhibition of foodborne pathogens by native microflora recovered from fresh peeled baby carrot and propagated in cultures. J Food Sci 72(4):M134–M139CrossRefGoogle Scholar
  94. Lindberg AM, Ljungh A, Ahrne S, Lofdahl S, Molin G (1998) Enterobacteriaceae found in high numbers in fish, minced meat and pasteurised milk or cream and the presence of toxin encoding genes. Int J Food Microbiol 39:11–17CrossRefGoogle Scholar
  95. Liu M, Griffths MW (2003) The role of QS in the regulation of protease by Pseudomonas fluorescens and its relation to food spoilage. Abstracts of Institute of Food Technologies Annual Meeting 2003. Institute of Food Technologists, Chicago, pp 85, 29G–26Google Scholar
  96. 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 69:2729–2737CrossRefGoogle Scholar
  97. Liu NT, Nou X, Lefcourt AM, Shelton DR, Lo YM (2014) Dual-species biofilm formation by Escherichia coli O157:H7 and environmental bacteria isolated from fresh-cut processing facilities. Intl J Food Microbiol 171:15–20CrossRefGoogle Scholar
  98. Liu Z, Pan Y, Li X, Jie J, Zeng M (2017) Chemical composition, antimicrobial and anti-QS activities of pummelo peel flavonoid extract. Ind Crop Prod 109:862–868CrossRefGoogle Scholar
  99. Llamas I, Keshavan N, Gonzalez JE (2004) Use of Sinorhizobium meliloti as an indicator for specific detection of long-chain N-acyl homoserine lactones. Appl Environ Microbiol 70:3715–3723PubMedCentralCrossRefPubMedGoogle Scholar
  100. Lourenco A, Machado H, Brito L (2011) Biofilms of Listeria monocytogenes produced at 12 °C either in pure culture or in co-culture with Pseudomonas aeruginosa showed reduced susceptibility to sanitizers. J Food Sci Chicago 76(2):M143–M148CrossRefGoogle Scholar
  101. Lu L, Hume ME, Pillai SD (2004) Autoinducer-2-like activity associated with foods and its interaction with food additives. J Food Prot 67:1457–1462PubMedCentralCrossRefPubMedGoogle Scholar
  102. Lu L, Hume ME, Pillai SD (2005) Autoinducer-2-like activity on vegetable produce and its potential involvement in bacterial biofilm formation on tomatoes. Foodborne Path Dis 2:242–249CrossRefGoogle Scholar
  103. Lund BM (1982) The effect of bacteria on post-harvest quality of vegetables and fruits, with particular reference to spoilage. Soc Appl Bacteriol Symp Ser 10:133–153Google Scholar
  104. Marouani-Gadri N, Augier G, Carpentier B (2009) Characterization of bacterial strains isolated from a beef-processing plant following cleaning and disinfection – influence of isolated strains on biofilm formation by Saka¨ı and EDL 933 E. coli O157:H7. Int J Food Microbiol 133(1–2):62–67CrossRefGoogle Scholar
  105. Medina-Martínez MS, Uyttendaele M, Meireman S, Debevere J (2006) Relevance of Nacyl-L-homoserine lactone production by Yersinia enterocolitica in fresh foods. J Appl Microbiol 102:1150–1158Google Scholar
  106. Medina-Martinez MS, Uyttendaele M, Meireman S, Debevere J (2007) Relevance of N-acyl-L-homoserine lactone production by Yersinia enterocolitica in fresh foods. J Appl Microbiol 102(4):1150–1158Google Scholar
  107. Millezi FM, Pereira MO, Batista NN, Camargos N, Auad I, Cardoso MDG, Piccoli RH (2012) Susceptibility of monospecies and dual-species biofilms of Staphylococcus aureus and Escherichia coli to essential oils. J Food Saf 32:351–359CrossRefGoogle Scholar
  108. Milton DL (2006) Quorum sensing in vibrios: complexity for diversification. Int J Med Microbiol 296:61–71CrossRefGoogle Scholar
  109. MMWR, Morbidity and Mortality Weekly Report (2005) Outbreaks of Salmonella Infections Associated with eating roma tomatoes—United States and Canada. MMWR 54(13):325–328.Google Scholar
  110. Møller S, Sternberg C, Andersen JB, Christensen BB, Ramos JL, Givskov M, Molin S (1998) In situ gene expression in mixed-species biofilms: evidence of metabolic interactions between community members. Appl Environ Microbiol 64(2):721–732PubMedCentralPubMedGoogle Scholar
  111. Moons P, Van Houdt R, Aertsen A, Vanoirbeek K, Engelborghs Y, Michiels CW (2006) Role of quorum sensing and antimicrobial component production by Serratia plymuthica in formation of biofilms, including. Appl Environ Microbiol 72(11):7294–7300PubMedCentralCrossRefPubMedGoogle Scholar
  112. Morin D, Grasland B, Vallée-Réhel K, Dufau C, Haras D (2003) On-line high performance liquid chromatography-mass spectrometric detection and quantification of N−acylhomoserine lactones, quorum sensing signal molecules, in the presence of biological matrices. J Chromatogr A 1002:79–92CrossRefGoogle Scholar
  113. National Institutes of Health, USA (1997) Minutes of the National Advisory Dental and Craniofacial Research Council—153rd Meeting, Bethesda, MDGoogle Scholar
  114. Nazzaro F, Fratianni F, Coppola R (2013) Quorum sensing and phyto-chemicals. Int J Mol Sci 14:12607–12619PubMedCentralCrossRefPubMedGoogle Scholar
  115. Niu C, Afre S, Gilbert ES (2006) Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett Appl Microbiol 43:489–494CrossRefGoogle Scholar
  116. Nychas G-JE, Skandamis P (2005) Fresh meat and modified atmosphere packaging (MAP). In: Sofos JN (ed) Improving the safety of fresh meat. Woodhead Publishing Ltd, Cambridge, pp 461–502CrossRefGoogle Scholar
  117. Nychas G-JE, Dillon VM, Board RG (1988) Glucose, the key substrate in the microbiological changes occurring in meat and certain meat products. Biotechnol Appl Biochem 10:203–231Google Scholar
  118. Oliveira BDÁ, Rodrigues AC, Cardoso BMI, Ramos ALCC, Bertoldi MC, Taylor JG et al (2016) Antioxidant, antimicrobial and anti-QS activities of Rubus rosaefolius phenolic extract. Ind Crop Prod 84:59–66CrossRefGoogle Scholar
  119. Ortori CA, Atkinson S, Chhabra SR, Cámara M, Williams P, Barrett DA (2007) Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole-linear ion trap mass spectrometry. Anal Bioanal Chem 387:497–511CrossRefGoogle Scholar
  120. Paggi RA, Martone CB, Fuqua C, de Castro RE (2003) Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus occultus. FEMS Microbiol Lett 221:49–52PubMedCentralCrossRefPubMedGoogle Scholar
  121. Pan Y, Breidt F, Kathariou S (2006) Resistance of Listeria monocytogenes biofilms to sanitizing agents in a stimulated food processing environment. Appl Environ Microbiol 72:7711–7717PubMedCentralCrossRefPubMedGoogle Scholar
  122. Pan Y, Breidt F Jr, Kathariou S (2009) Competition of Listeria monocytogenes serotype 1/2a and 4b strains in mixed-species biofilms. Appl Environ Microbiol 75(18):5846–5852PubMedCentralCrossRefPubMedGoogle Scholar
  123. Parlapani FF, Haroutounian SA, Nychas GJ, Boziaris IS (2015 Sep 1) Microbiological spoilage and volatiles production of gutted European sea bass stored under air and commercial modified atmosphere package at 2 C. Food Microbiol 50:44–53CrossRefGoogle Scholar
  124. Patel CN, Wortham BW, Lines JL, Fetherston JD, Perry RD, Oliveira MA (2006 Apr 1) Polyamines are essential for the formation of plague biofilm. J Bacteriol 188(7):2355–2363PubMedCentralCrossRefPubMedGoogle Scholar
  125. Percival SL, Walker JT, Hunter PR (2000) Microbiological aspects on biofilms and drinking water. CRC Press, Boca RatonCrossRefGoogle Scholar
  126. Persson T, Hansen TH, Rasmussen TB, Skinderso ME, Givskov M, Nielsen J (2005) Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org Biomol Chem 3:253–262PubMedCentralCrossRefPubMedGoogle Scholar
  127. Ponnusamy K, Paul D, Kweon JH (2009) Inhibition of quorum sensing mechanism and Aeromonas hydrophila biofilm formation by vanillin. Environ Eng Sci 26(8):1359–1363CrossRefGoogle Scholar
  128. Rangel JM, Sparling PH, Crowe C, Griffin PM, Swerdlow DL (2005) Epidemiology of Escherichia coli outbreaks, United States, 1982–2002. Emerg Infect Dis 11:603–609PubMedCentralCrossRefPubMedGoogle Scholar
  129. 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 71:3321–3330PubMedCentralCrossRefPubMedGoogle Scholar
  130. Ren D, Sims JJ, Wood TK (2001) Inhibition of biofilm formation and swarming of Escherichia coli by (5Z) -4-bromo-5-(bromomethylene) -3-butyl-2 (5H) -furanone. Environ Microbiol 3(11):731–736CrossRefGoogle Scholar
  131. Ren D, Madsen JS, Cruz-Perera CI, Bergmark L, Sørensen SJ, Burmølle M (2013) High-throughput screening of multispecies biofilm formation and quantitative PCR-based assessment of individual species proportions, useful for exploring interspecific bacterial interactions. Microb Ecol. Scholar
  132. Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A, Wu H, Høiby N, Givskov M, Molin S, Eberl L (2001 Dec 1) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147(12):3249–3262CrossRefGoogle Scholar
  133. Rieu A, Lemaˆıtre JP, Guzzo J, Piveteau P (2008) Interactions in dual species biofilms between Listeria monocytogenes EGD-e and several strains of Staphylococcus aureus. Intl J Food Microbiol 126(1–2):76–82CrossRefGoogle Scholar
  134. Rivas M, Seeger M, Jedlicki E, Holmes DS (2007) Second acylhomoserine lactone-producing system in the extreme acidophile Acidithiobacillus ferrooxidans. Appl Environ Microbiol 73:3225–3231PubMedCentralCrossRefPubMedGoogle Scholar
  135. Romero M, Martin-Cuadrado AB, Roca-Rivada A, Cabello AM, Otero A (2011) Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol Ecol 75:205–217PubMedCentralCrossRefPubMedGoogle Scholar
  136. Ryan KJ, Ray CG (eds) (2004) Sherris medical microbiology, 4th edn. McGraw Hill. ISBN 0-8385-8529-9
  137. Sanders SQ, Frank JF, Arnold JW (2008) Temperature and nutrient effects on Campylobacter jejuni attachment on multispecies biofilms on stainless steel. J Food Prot 71(2):271–278CrossRefGoogle Scholar
  138. Schwering M, Song J, Louie M, Turner RJ, Ceri H (2013) Multi-species biofilms defined from drinking water microorganisms provide increased protection against chlorine disinfection. Biofouling 29(8):917–928CrossRefGoogle Scholar
  139. Sela S, Frank S, Belausov E, Pinto R (2006) A mutation in the luxS gene influences Listeria monocytogenes biofilm formation. Appl Environ Microbiol 72:5653–5658PubMedCentralCrossRefPubMedGoogle Scholar
  140. Shao CP, Hor LI (2001) Regulation of metalloprotease gene expression in Vibrio vulnificus by a Vibrio harveyi LuxR homologue. J Bacteriol 183:1369–1375PubMedCentralCrossRefPubMedGoogle Scholar
  141. Shen C, Luo Y, Nou X, Bauchan G, Zhou B, Wang Q, Millner P (2012) Enhanced inactivation of Salmonella and Pseudomonas biofilms on stainless steel by use of T-128, a fresh-produce washing aid, in chlorinated wash solutions. Appl Environ Microbiol 78(19):6789–6798PubMedCentralCrossRefPubMedGoogle Scholar
  142. Silagyi K, Kim SH, Lo YM, Wei CI (2009) Production of biofilm and quorum sensing by Escherichia coli O157: H7 and its transfer from contact surfaces to meat, poultry, ready-to-eat deli, and produce products. Food Microbiol 26(5):514–519CrossRefGoogle Scholar
  143. Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV (2004) Fresh produce; a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 67:2342–2353CrossRefGoogle Scholar
  144. Slamti L, Lereclus D (2002) A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 21:4550–4559PubMedCentralCrossRefPubMedGoogle Scholar
  145. Slamti L, Lereclus D (2005) Specificity and polymorphism of the PlcR-PapR quorum sensing system in the Bacillus cereus group. J Bacteriol 187:1182–1187PubMedCentralCrossRefPubMedGoogle Scholar
  146. Smith JL, Fratamico PM, Novak JS (2004) QS: a primer for food microbiologists. J Food Prot 67:1053–1070CrossRefGoogle Scholar
  147. Solomon EB, Niemira BA, Sapers GM, Annous BA (2005) Biofilm formation, cellulose production, and curli biosynthesis by Salmonella originating from produce, animal and clinical sources. J Food Prot 68:906–912CrossRefGoogle Scholar
  148. Soni KA, Jesudhasan P, Cepeda M, Widmer K, Jayaprakasha GK, Patil BS, Hume ME, Pillai SD (2008) Identification of ground beef derived fatty acid inhibitors of autoinducer-2 based cell signaling. J Food Prot 71:134–138CrossRefGoogle Scholar
  149. Sutherland IW (2001) The biofilm matrix ̶ an immobilized but dynamic microbial environment. Trends Microbiol 9:222–227PubMedCentralCrossRefPubMedGoogle Scholar
  150. Tang K, Zhang XH (2014) Quorum quenching agents: resources for antivirulence therapy. Mar Drugs 12(6):3245–3282PubMedCentralCrossRefPubMedGoogle Scholar
  151. Teh KH, Flint S, French N (2010) Biofilm formation by Campylobacter jejuni in controlled mixed-microbial populations. Intl J Food Microbiol 143(3):118–124CrossRefGoogle Scholar
  152. Tenaillon O, Skurnik D, Picard B, Denamur E (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8(3):207–217. ISSN 1740-1526CrossRefGoogle Scholar
  153. Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GP (2000 May) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36(3):539–556CrossRefGoogle Scholar
  154. Tristezza M, Lourenco A, Barata A, Brito L, Malfeito-Ferreira M, Loureiro V (2010) Susceptibility of wine spoilage yeasts and bacteria in the planktonic state and in biofilms to disinfectants. Ann Microbiol 60:549–556CrossRefGoogle Scholar
  155. Uhlich GA, Rogers DP, Mosier DA (2010) Escherichia coli serotype O157: H7 retention on solid surfaces and peroxide resistance is enhanced by dual-strain biofilm formation. Foodborne Pathog Dis 7(8):935–943CrossRefGoogle Scholar
  156. van der Veen S, Abee T (2011) Mixed-species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. Intl J Food Microbiol 144(3):421–431CrossRefGoogle Scholar
  157. Van Houdt R, Aertsen A, Jansen A, Quintana AL, Michiels CW (2004) Biofilm formation and cell-to-cell signalling in Gram-negative bacteria isolated from a food processing environment. J Appl Microbiol 96:177–184CrossRefGoogle Scholar
  158. Van Houdt R, Moons P, Buj MH, Michiels CW (2006 Jun 15) N-acyl-L-homoserine lactone quorum sensing controls butanediol fermentation in Serratia plymuthica RVH1 and Serratia marcescens MG1. J Bacteriol 188(12):4570–4572PubMedCentralCrossRefPubMedGoogle Scholar
  159. Van Houdt R, Moons P, Aertsen A, Jansen A, Vanoirbeek K, Daykin M, Williams P, Michiels CW (2007) Characterization of a luxI/luxR-type quorum sensing system and N-acyl-homoserine lactone–dependent regulation of exo-enzyme and antibacterial component production in Serratia plymuthica RVH1. Res Microbiol 158:150–158CrossRefGoogle Scholar
  160. Vattem DA, Mihalik K, Crixell SH, McLean RJC (2007) Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78(4):302–310PubMedCentralCrossRefPubMedGoogle Scholar
  161. Venkadesaperumal G, Rucha S, Sundar K, Shetty PH (2016) Anti-QS activity of spice oil nanoemulsions against food borne pathogens. LWT Food Sci Technol 66:225–231CrossRefGoogle Scholar
  162. Vogt RL, Dippold L (2005) Escherichia coli O157:H7 outbreak associated with consumption of ground beef, June–July 2002. Publ Health Rep 120(2):174–178. PMC 1497708. PMID 15842119PubMedCentralCrossRefPubMedGoogle Scholar
  163. Wang H-H, Ye K-P, Zhang Q-Q, Yang D, Xu X-L, Zhou G-H (2013a) Biofilm formation of meat-borne Salmonella enterica and inhibition by the cell-free supernatant from Pseudomonas aeruginosa. Food Control 32:650–658CrossRefGoogle Scholar
  164. Wang R, Kalchayanand N, Schmidt JW, Harhay DM (2013b) Mixed biofilm formation by Shiga toxin-producing Escherichia coli and Salmonella enterica serovar Typhimurium enhanced bacterial resistance to sanitization due to extracellular polymeric substances. J Food Prot 76(9):1513–1522CrossRefPubMedPubMedCentralGoogle Scholar
  165. Wang F, Fu L, Bao X, Wang Y (2017) The spoilage microorganisms in seafood with the existed quorum sensing phenomenon. J Food Microbiol 1(1)Google Scholar
  166. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346PubMedCentralCrossRefPubMedGoogle Scholar
  167. Whan L, Dunstall G, Rowe MT (2000) A study of the growth kinetics of two pseudomonads from pasteurized milk and the possible role of quorum sensing. Milchwissenschaft 55:371–373Google Scholar
  168. Whitfield FB, Jensen N, Shaw KJ (2000 Nov) Role of Yersinia intermedia and Pseudomonas putida in the development of a fruity off-flavour in pasteurized milk. J Dairy Res 67(4):561–569CrossRefGoogle Scholar
  169. World Health Organization (WHO) (2011) Global Foodborne Infections Network (GFN).
  170. World Health Organization (WHO) (2012) Initiative to estimate the Global Burden of Foodborne Diseases.
  171. Yarwood JM, Schlievert PM (2003) QS in Staphylococcus infections. J Clin Invest 112:1620–1625PubMedCentralCrossRefPubMedGoogle Scholar
  172. Yoon Y, Sofos JN (2008) Autoinducer-2 activity of gram-negative foodborne pathogenic bacteria and its influence on biofilm formation. J Food Sci 73:M140–M147CrossRefGoogle Scholar
  173. Zameer F, Kreft J, Gopal S (2010) Interaction of Listeria monocytogenes and Staphylococcus epidermis in dual species biofilms. J Food Saf 30:954–968CrossRefGoogle Scholar
  174. Zhang QQ, Ye KP, Wang HH, Xiao HM, Xu XL, Zhou GH (2014) Inhibition of biofilm formation of Pseudomonas aeruginosa by an acylated homoserine lactones-containing culture extract. LWT Food Sci Technol 57:230–235CrossRefGoogle Scholar
  175. Zhang C, Zhu S, Jatt AN, Pan Y, Zeng M (2017) Proteomic assessment of the role of N-acyl homoserine lactone in Shewanella putrefaciens spoilage. Lett Appl Microbiol 65(5):388–394CrossRefGoogle Scholar
  176. Zhao T, Doyle MP, Zhao P (2004) Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Appl Environ Microbiol 70:3996–4003PubMedCentralCrossRefPubMedGoogle Scholar
  177. Zhao D, Lyu F, Liu S, Zhang J, Ding Y, Chen W, Zhou X (2017a) Involvement of bacterial quorum sensing signals in spoilage potential of Aeromonas veronii bv. veronii isolated from fermented surimi. J Food Biochem 42:e12487CrossRefGoogle Scholar
  178. Zhao X, Zhao F, Wang J, Zhong N (2017b) Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Adv 7(58):36670–36683CrossRefGoogle Scholar
  179. 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 192:26–33CrossRefGoogle Scholar
  180. Zhu S, Zhang C, Wu H, Jie J, Zeng M, Liu Z et al (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):1517–1526CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Saqib Hassan
    • 1
  • Tanveer Ahmad
    • 2
  • Mudasir Bashir
    • 3
  • G. Seghal Kiran
    • 3
  • Joseph Selvin
    • 4
    Email author
  1. 1.Department of MedicineImperial College LondonLondonUK
  2. 2.Department of Biotechnology, School of Life SciencesPondicherry UniversityPuducherryIndia
  3. 3.Department of Food Science and Technology, School of Life SciencesPondicherry UniversityPuducherryIndia
  4. 4.Department of Microbiology, School of Life SciencesPondicherry UniversityPuducherryIndia

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