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Quorum Sensing Complexity of the Gut Enterobacteria Escherichia coli and Salmonella enterica

  • Chandrajit LahiriEmail author
Chapter

Abstract

The human alimentary canal is the reservoir of a diverse range of bacteria, of which the gram negative strains of Escherichia coli and Salmonella enterica mostly present themselves as beneficial and opportunistic pathogens, respectively. The complex environment of the human gut necessitates an adaptation by these bacterial species, which, primarily, is done through interspecies communication mediated by cell-density dependent gene regulation. This phenotype of sensing the quorum a.k.a. quorum sensing (QS), has been shown to play roles in bioluminescence, formation of biofilm, swarming motility and virulence for bacterial species over the years. For E. coli and S. enterica, quorum sensing (QS) a.k.a. intracellular signalling has been mediated by more than one mechanistic pathway involving the proteins and biomolecules such as the autoinducer-1 (AI-1) type LuxR homolog SdiA, AI-2 type LuxS, AI-3 type epinephrine/norepinephrine and/or indole. A usage of these proteins and/or biochemicals in combination is a hint towards their adaption to the influencing factors in the external environmental milieu of the host human gut. Notably, high osmolarity, low or neutral pH and preferred carbon sources affect such adaptation processes. While numerous bioactive compounds like Artemisin, Digoxin, Flavonoids, Ginkgo, Phenols, Punicalagin, Stilbene, Taxol, Vincristine and Vinblastine act as anti-QS products and have been explored, novel brominated N-heterocycles have started gaining importance as new measure for the antimicrobial resistance threats posed by such Enterobacteriaciae.

Keywords

Escherichia Salmonella Quorum sensing LuxS AI-1 AI-2 

Notes

Acknowledgments

The author acknowledges the support of Sunway University, Selangor, Malaysia for providing the computational facilities and wishes to thank Rohit Mishra for the valuable contribution in developing the art work for the concept provided.

References

  1. 1.
    Thursby, E., & Juge, N. (2017). Introduction to the human gut microbiota. Biochemical Journal, 474(11), 1823–1836.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Hugon, P., Dufour, J. C., Colson, P., Fournier, P. E., Sallah, K., & Raoult, D. (2015). A comprehensive repertoire of prokaryotic species identified in human beings. The Lancet Infectious Diseases, 15(10), 1211–1219.PubMedCrossRefGoogle Scholar
  3. 3.
    Li, J., Jia, H., Cai, X., Zhong, H., Feng, Q., Sunagawa, S., ..., Juncker, A. S. (2014a). An integrated catalog of reference genes in the human gut microbiome. Nature biotechnology, 32(8), 834.PubMedCrossRefGoogle Scholar
  4. 4.
    Ng, K. M., Ferreyra, J. A., Higginbottom, S. K., Lynch, J. B., Kashyap, P. C., Gopinath, S., ..., Sonnenburg, J. L. (2013). Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature, 502(7469), 96.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Huang, Y. L., Chassard, C., Hausmann, M., Von Itzstein, M., & Hennet, T. (2015). Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice. Nature Communications, 6, 8141.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Tomasz, A. (1965). Control of the competent state in pneumococcus by a hormone-like cell product: An example for a new type of regulatory mechanism in bacteria. Nature, 208(5006), 155.PubMedCrossRefGoogle Scholar
  7. 7.
    Nealson, K. H., Platt, T., & Hastings, J. W. (1970). Cellular control of the synthesis and activity of the bacterial luminescent system. Journal of Bacteriology, 104(1), 313–322.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Walters, M., & Sperandio, V. (2006). Quorum sensing in Escherichia coli and Salmonella. International Journal of Medical Microbiology, 296(2–3), 125–131.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Choi, J., Shin, D., & Ryu, S. (2007). Implication of quorum sensing in Salmonella enterica serovar typhimurium virulence: The luxS gene is necessary for expression of genes in pathogenicity island 1. Infection and Immunity, 75(10), 4885–4890.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Sturbelle, R. T., de Avila, L. F. D. C., Roos, T. B., Borchardt, J. L., Dellagostin, O. A., & Leite, F. P. L. (2015). The role of quorum sensing in Escherichia coli (ETEC) virulence factors. Veterinary Microbiology, 180(3–4), 245–252.PubMedCrossRefGoogle Scholar
  11. 11.
    Pawar, S., & Lahiri, C. (2018). Quorum sensing: An imperative longevity weapon in bacteria. African Journal of Microbiology Research, 12(4), 96–104.CrossRefGoogle Scholar
  12. 12.
    Surette, M. G., & Bassler, B. L. (1998). Quorum sensing in Escherichia coli and Salmonella typhimurium. Proceedings of the National Academy of Sciences, 95(12), 7046–7050.CrossRefGoogle Scholar
  13. 13.
    Surette, M. G., & Bassler, B. L. (1999). Regulation of autoinducer production in Salmonella typhimurium. Molecular Microbiology, 31(2), 585–595.PubMedCrossRefGoogle Scholar
  14. 14.
    Surette, M. G., Miller, M. B., & Bassler, B. L. (1999). Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: A new family of genes responsible for autoinducer production. Proceedings of the National Academy of Sciences, 96(4), 1639–1644.CrossRefGoogle Scholar
  15. 15.
    Maloy, S. R., Stewart, V. J., & Taylor, R. K. (1996). Genetic analysis of pathogenic bacteria: A laboratory manual. Plainview: Cold Spring Harbor Laboratory Press.Google Scholar
  16. 16.
    Blattner, F. R., Plunkett, G., Bloch, C. A., Perna, N. T., Burland, V., Riley, M., ..., Gregor, J. (1997). The complete genome sequence of Escherichia coli K-12. Science, 277(5331), 1453–1462.PubMedCrossRefGoogle Scholar
  17. 17.
    Cloak, O. M., Solow, B. T., Briggs, C. E., Chen, C. Y., & Fratamico, P. M. (2002). Quorum sensing and production of autoinducer-2 in Campylobacter spp., Escherichia coli O157: H7, and Salmonella enterica serovar Typhimurium in foods. Applied and Environmental Microbiology, 68(9), 4666–4671.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B. L., & Hughson, F. M. (2002). Structural identification of a bacterial quorum-sensing signal containing boron. Nature, 415(6871), 545.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Miller, S. T., Xavier, K. B., Campagna, S. R., Taga, M. E., Semmelhack, M. F., Bassler, B. L., & Hughson, F. M. (2004). Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Molecular Cell, 15(5), 677–687.PubMedCrossRefGoogle Scholar
  20. 20.
    Taga, M. E., Semmelhack, J. L., & Bassler, B. L. (2001). The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Molecular Microbiology, 42(3), 777–793.PubMedCrossRefGoogle Scholar
  21. 21.
    Taga, M. E., Miller, S. T., & Bassler, B. L. (2003). Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Molecular Microbiology, 50(4), 1411–1427.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Soares, J. A., & Ahmer, B. M. (2011). Detection of acyl-homoserine lactones by Escherichia and Salmonella. Current Opinion in Microbiology, 14(2), 188–193.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Fuqua, W. C., Winans, S. C., & Greenberg, E. P. (1994). Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. Journal of Bacteriology, 176(2), 269.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Kaplan, H. B., & Greenberg, E. P. (1985). Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. Journal of Bacteriology, 163(3), 1210–1214.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Pearson, J. P., Van Delden, C., & Iglewski, B. H. (1999). Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. Journal of Bacteriology, 181(4), 1203–1210.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Case, R. J., Labbate, M., & Kjelleberg, S. (2008). AHL-driven quorum-sensing circuits: Their frequency and function among the Proteobacteria. The ISME Journal, 2(4), 345.CrossRefGoogle Scholar
  27. 27.
    de Almeida, F. A., Pinto, U. M., & Vanetti, M. C. D. (2016). Novel insights from molecular docking of SdiA from Salmonella Enteritidis and Escherichia coli with quorum sensing and quorum quenching molecules. Microbial Pathogenesis, 99, 178–190.PubMedCrossRefGoogle Scholar
  28. 28.
    Ahmer, B. M., Van Reeuwijk, J., Timmers, C. D., Valentine, P. J., & Heffron, F. (1998). Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. Journal of Bacteriology, 180(5), 1185–1193.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Sitnikov, D. M., Schineller, J. B., & Baldwin, T. O. (1996). Control of cell division in Escherichia coli: Regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction. Proceedings of the National Academy of Sciences, 93(1), 336–341.CrossRefGoogle Scholar
  30. 30.
    Michael, B., Smith, J. N., Swift, S., Heffron, F., & Ahmer, B. M. (2001). SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. Journal of Bacteriology, 183(19), 5733–5742.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Smith, J. N., & Ahmer, B. M. (2003). Detection of other microbial species by Salmonella: Expression of the SdiA regulon. Journal of Bacteriology, 185(4), 1357–1366.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Smith, J. N., Dyszel, J. L., Soares, J. A., Ellermeier, C. D., Altier, C., Lawhon, S. D., ..., Ahmer, B. M. (2008). SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS One, 3(7), e2826.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Dyszel, J. L., Soares, J. A., Swearingen, M. C., Lindsay, A., Smith, J. N., & Ahmer, B. M. (2010b). E. coli K-12 and EHEC genes regulated by SdiA. PLoS One, 5(1), e8946.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Doğaner, B. A., Yan, L. K., & Youk, H. (2016). Autocrine signaling and quorum sensing: Extreme ends of a common spectrum. Trends in Cell Biology, 26(4), 262–271.PubMedCrossRefGoogle Scholar
  35. 35.
    Nesse, L. L., Berg, K., Vestby, L. K., Olsaker, I., & Djønne, B. (2011). Salmonella typhimurium invasion of HEp-2 epithelial cells in vitro is increased by N-acylhomoserine lactone quorum sensing signals. Acta Veterinaria Scandinavica, 53(1), 44.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Liu, Z., Que, F., Liao, L., Zhou, M., You, L., Zhao, Q., ..., Huang, R. (2014). Study on the promotion of bacterial biofilm formation by a salmonella conjugative plasmid and the underlying mechanism. PloS one, 9(10), e109808.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Campos Galvão, M. E. M., Ribon, A. O. B., Araújo, E. F., & Vanetti, M. C. D. (2016). Changes in the Salmonella enterica Enteritidis phenotypes in presence of acyl homoserine lactone quorum sensing signals. Journal of Basic Microbiology, 56(5), 493–501.PubMedCrossRefGoogle Scholar
  38. 38.
    Van Houdt, R., Aertsen, A., Moons, P., Vanoirbeek, K., & Michiels, C. W. (2006). N-acyl-L-homoserine lactone signal interception by Escherichia coli. FEMS Microbiology Letters, 256(1), 83–89.PubMedCrossRefGoogle Scholar
  39. 39.
    Lee, J., Maeda, T., Hong, S. H., & Wood, T. K. (2009). Reconfiguring the quorum-sensing regulator SdiA of Escherichia coli to control biofilm formation via indole and N-acylhomoserine lactones. Applied and Environmental Microbiology, 75(6), 1703–1716.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Sharma, V. K., & Bearson, S. M. D. (2013). Evaluation of the impact of quorum sensing transcriptional regulator SdiA on long-term persistence and fecal shedding of Escherichia coli O157: H7 in weaned calves. Microbial Pathogenesis, 57, 21–26.PubMedCrossRefGoogle Scholar
  41. 41.
    de Almeida, F. A., de Jesus Pimentel-Filho, N., Pinto, U. M., Mantovani, H. C., de Oliveira, L. L., & Vanetti, M. C. D. (2017b). Acyl homoserine lactone-based quorum sensing stimulates biofilm formation by Salmonella Enteritidis in anaerobic conditions. Archives of Microbiology, 199(3), 475–486.PubMedCrossRefGoogle Scholar
  42. 42.
    de Almeida, F. A., de Jesus Pimentel-Filho, N., Carrijo, L. C., Bento, C. B. P., Baracat-Pereira, M. C., Pinto, U. M., ..., Vanetti, M. C. D. (2017a). Acyl homoserine lactone changes the abundance of proteins and the levels of organic acids associated with stationary phase in Salmonella Enteritidis. Microbial Pathogenesis, 102, 148–159.PubMedCrossRefGoogle Scholar
  43. 43.
    Dyszel, J. L., Smith, J. N., Lucas, D. E., Soares, J. A., Swearingen, M. C., Vross, M. A., ..., Ahmer, B. M. (2010a). Salmonella enterica serovar Typhimurium can detect acyl homoserine lactone production by Yersinia enterocolitica in mice. Journal of Bacteriology, 192(1), 29–37.PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Nguyen, Y., Nguyen, N. X., Rogers, J. L., Liao, J., MacMillan, J. B., Jiang, Y., & Sperandio, V. (2015). Structural and mechanistic roles of novel chemical ligands on the SdiA quorum-sensing transcription regulator. MBio, 6(2), e02429–e02414.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Hughes, D. T., Terekhova, D. A., Liou, L., Hovde, C. J., Sahl, J. W., Patankar, A. V., ..., Sperandio, V. (2010). Chemical sensing in mammalian host–bacterial commensal associations. Proceedings of the National Academy of Sciences, 107(21), 9831–9836.CrossRefGoogle Scholar
  46. 46.
    Alvarez, H., & Steinbüchel, A. (2002). Triacylglycerols in prokaryotic microorganisms. Applied Microbiology and Biotechnology, 60(4), 367–376.PubMedCrossRefGoogle Scholar
  47. 47.
    Liu, Q., Siloto, R. M., Lehner, R., Stone, S. J., & Weselake, R. J. (2012). Acyl-CoA: Diacylglycerol acyltransferase: Molecular biology, biochemistry and biotechnology. Progress in Lipid Research, 51(4), 350–377.PubMedCrossRefGoogle Scholar
  48. 48.
    Abed, N., Grépinet, O., Canepa, S., Hurtado-Escobar, G. A., Guichard, N., Wiedemann, A., ..., Virlogeux-Payant, I. (2014). Direct regulation of the pefI-srgC operon encoding the Rck invasin by the quorum-sensing regulator SdiA in Salmonella Typhimurium. Molecular microbiology, 94(2), 254–271.PubMedCrossRefGoogle Scholar
  49. 49.
    Velge, P., Wiedemann, A., Rosselin, M., Abed, N., Boumart, Z., Chausse, A. M., ..., Virlogeux Payant, I. (2012). Multiplicity of Salmonella entry mechanisms, a new paradigm for Salmonella pathogenesis. Microbiology, 1(3), 243–258.Google Scholar
  50. 50.
    Ly, K. T., & Casanova, J. E. (2007). Mechanisms of Salmonella entry into host cells. Cellular Microbiology, 9(9), 2103–2111.PubMedCrossRefGoogle Scholar
  51. 51.
    Rosselin, M., Virlogeux-Payant, I., Roy, C., Bottreau, E., Sizaret, P. Y., Mijouin, L., ..., Wiedemann, A. (2010). Rck of Salmonella enterica, subspecies enterica serovar Enteritidis, mediates Zipper-like internalization. Cell research, 20(6), 647.PubMedCrossRefGoogle Scholar
  52. 52.
    Heffernan, E. J., Harwood, J., Fierer, J., & Guiney, D. (1992). The Salmonella typhimurium virulence plasmid complement resistance gene rck is homologous to a family of virulence-related outer membrane protein genes, including pagC and ail. Journal of Bacteriology, 174(1), 84–91.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Karavolos, M. H., Bulmer, D. M., Winzer, K., Wilson, M., Mastroeni, P., Williams, P., & Khan, C. M. A. (2008). LuxS affects flagellar phase variation independently of quorum sensing in Salmonella enterica serovar Typhimurium. Journal of Bacteriology, 190(2), 769–771.PubMedCrossRefGoogle Scholar
  54. 54.
    Bonifield, H. R., & Hughes, K. T. (2003). Flagellar phase variation in Salmonella enterica is mediated by a posttranscriptional control mechanism. Journal of Bacteriology, 185(12), 3567–3574.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Yamamoto, S., & Kutsukake, K. (2006). FljA-mediated posttranscriptional control of phase 1 flagellin expression in flagellar phase variation of Salmonella enterica serovar Typhimurium. Journal of Bacteriology, 188(3), 958–967.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Jones, B. D., Lee, C. A., & Falkow, S. T. A. N. L. E. Y. (1992). Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infection and Immunity, 60(6), 2475–2480.PubMedPubMedCentralGoogle Scholar
  57. 57.
    La Ragione, R. M., Cooley, W. A., Velge, P., Jepson, M. A., & Woodward, M. J. (2003). Membrane ruffling and invasion of human and avian cell lines is reduced for aflagellate mutants of Salmonella enterica serotype Enteritidis. International Journal of Medical Microbiology, 293(4), 261–272.PubMedCrossRefGoogle Scholar
  58. 58.
    Steiner, T. S. (2007). How flagellin and toll-like receptor 5 contribute to enteric infection. Infection and Immunity, 75, 545–552.PubMedCrossRefGoogle Scholar
  59. 59.
    Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T. D., Özören, N., Jagirdar, R., ..., Grant, E. P. (2006). Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infected macrophages. Nature Immunology, 7(6), 576.PubMedCrossRefGoogle Scholar
  60. 60.
    Miao, E. A., Alpuche-Aranda, C. M., Dors, M., Clark, A. E., Bader, M. W., Miller, S. I., & Aderem, A. (2006). Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf. Nature Immunology, 7(6), 569.PubMedCrossRefGoogle Scholar
  61. 61.
    Yoon, Y., & Sofos, J. N. (2010). Absence of association of autoinducer-2-based quorum sensing with heat and acid resistance of Salmonella. Journal of Food Science, 75(7).PubMedCrossRefGoogle Scholar
  62. 62.
    Huang, C. T., & Shih, P. C. (2000). Effects of quorum sensing signal molecules on the hydrogen peroxide resistance against planktonic Pseudomonas aeruginosa. Journal of Microbiology, Immunology, and Infection Wei mian yu gan ran za zhi, 33(3), 154–158.PubMedGoogle Scholar
  63. 63.
    McDougald, D., Rice, S. A., & Kjelleberg, S. (2001). SmcR-dependent regulation of adaptive phenotypes in vibrio vulnificus. Journal of Bacteriology, 183(2), 758–762.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    McDougald, D., Srinivasan, S., Rice, S. A., & Kjelleberg, S. (2003). Signal-mediated cross-talk regulates stress adaptation in Vibrio species. Microbiology, 149(7), 1923–1933.PubMedCrossRefGoogle Scholar
  65. 65.
    Wen, Z. T., & Burne, R. A. (2004). LuxS-mediated signaling in Streptococcus mutans is involved in regulation of acid and oxidative stress tolerance and biofilm formation. Journal of Bacteriology, 186(9), 2682–2691.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Yao, Y., Vuong, C., Kocianova, S., Villaruz, A. E., Lai, Y., Sturdevant, D. E., & Otto, M. (2006). Characterization of the Staphylococcus epidermidis accessory-gene regulator response: Quorum-sensing regulation of resistance to human innate host defense. The Journal of Infectious Diseases, 193(6), 841–848.PubMedCrossRefGoogle Scholar
  67. 67.
    Choi, J., Shin, D., Kim, M., Park, J., Lim, S., & Ryu, S. (2012). LsrR-mediated quorum sensing controls invasiveness of Salmonella typhimurium by regulating SPI-1 and flagella genes. PLoS One, 7(5), e37059.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Clarke, M. B., & Sperandio, V. (2005). Events at the host-microbial interface of the gastrointestinal tract III. Cell-to-cell signaling among microbial flora, host, and pathogens: There is a whole lot of talking going on. American Journal of Physiology. Gastrointestinal and Liver Physiology, 288(6), G1105–G1109.PubMedCrossRefGoogle Scholar
  69. 69.
    Furness, J. B. (2000). Types of neurons in the enteric nervous system. Journal of the Autonomic Nervous System, 81(1), 87–96.PubMedCrossRefGoogle Scholar
  70. 70.
    Bearson, B. L., Bearson, S. M. D. (2007). The QseBC quorum sensing system is involved in Salmonella enterica serovar typhimurium colonization of the swine gastrointestinal tract. Digital Repository of Iowa State University, USA.Google Scholar
  71. 71.
    Dourou, D., Ammor, M. S., Skandamis, P. N., & Nychas, G. J. E. (2011). Growth of Salmonella enteritidis and Salmonella typhimurium in the presence of quorum sensing signalling compounds produced by spoilage and pathogenic bacteria. Food Microbiology, 28(5), 1011–1018.PubMedCrossRefGoogle Scholar
  72. 72.
    Lamas, A., Miranda, J. M., Vázquez, B., Cepeda, A., & Franco, C. M. (2016). Biofilm formation, phenotypic production of cellulose and gene expression in Salmonella enterica decrease under anaerobic conditions. International Journal of Food Microbiology, 238, 63–67.PubMedCrossRefGoogle Scholar
  73. 73.
    Zarrineh, P., Sánchez-Rodríguez, A., Hosseinkhan, N., Narimani, Z., Marchal, K., & Masoudi-Nejad, A. (2014). Genome-scale co-expression network comparison across Escherichia coli and Salmonella enterica serovar Typhimurium reveals significant conservation at the regulon level of local regulators despite their dissimilar lifestyles. PLoS One, 9(8), e102871.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Swofford, C. A., Van Dessel, N., & Forbes, N. S. (2015). Quorum-sensing Salmonella selectively trigger protein expression within tumors. Proceedings of the National Academy of Sciences, 112(11), 3457–3462.CrossRefGoogle Scholar
  75. 75.
    Park, H., Yeo, S., Ji, Y., Lee, J., Yang, J., Park, S., ..., Holzapfel, W. (2014). Autoinducer-2 associated inhibition by Lactobacillus sakei NR28 reduces virulence of enterohaemorrhagic Escherichia coli O157: H7. Food Control, 45, 62–69.CrossRefGoogle Scholar
  76. 76.
    Park, H., Shin, H., Lee, K., & Holzapfel, W. (2016). Autoinducer-2 properties of kimchi are associated with lactic acid bacteria involved in its fermentation. International Journal of Food Microbiology, 225, 38–42.PubMedCrossRefGoogle Scholar
  77. 77.
    Givskov, M., de Nys, R., Manefield, M., Gram, L., Maximilien, R. I. A., Eberl, L. E. O., ..., Kjelleberg, S. (1996). Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. Journal of Bacteriology, 178(22), 6618–6622.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Gram, L., de Nys, R. O. C. K. Y., Maximilien, R. I. A., Givskov, M., Steinberg, P., & Kjelleberg, S. (1996). Inhibitory effects of secondary metabolites from the red alga Delisea pulchra on swarming motility of Proteus mirabilis. Applied and Environmental Microbiology, 62(11), 4284–4287.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Iskander, G., Zhang, R., Chan, D. S. H., Black, D. S., Alamgir, M., & Kumar, N. (2009). An efficient synthesis of brominated 4-alkyl-2 (5H)-furanones. Tetrahedron Letters, 50(32), 4613–4615.CrossRefGoogle Scholar
  80. 80.
    Steenackers, H. P., Levin, J., Janssens, J. C., De Weerdt, A., Balzarini, J., Vanderleyden, J., ..., De Keersmaecker, S. C. (2010). Structure–activity relationship of brominated 3-alkyl-5-methylene-2 (5H)-furanones and alkyl maleic anhydrides as inhibitors of Salmonella biofilm formation and quorum sensing regulated bioluminescence in Vibrio harveyi. Bioorganic & Medicinal Chemistry, 18(14), 5224–5233.CrossRefGoogle Scholar
  81. 81.
    Steenackers, H. P., Ermolat’ev, D. S., Savaliya, B., De Weerdt, A., De Coster, D., Shah, A., ..., De Keersmaecker, S. C. (2011). Structure-activity relationship of 2-hydroxy-2-aryl-2, 3-dihydro-imidazo [1, 2-a] pyrimidinium salts and 2N-substituted 4 (5)-aryl-2-amino-1H-imidazoles as inhibitors of biofilm formation by Salmonella Typhimurium and Pseudomonas aeruginosa. Bioorganic & medicinal chemistry, 19(11), 3462–3473.CrossRefGoogle Scholar
  82. 82.
    Garner, A. L., Park, J., Zakhari, J. S., Lowery, C. A., Struss, A. K., Sawada, D., ..., Janda, K. D. (2011). A multivalent probe for AI-2 quorum-sensing receptors. Journal of the American Chemical Society, 133(40), 15934–15937.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Lowery, C. A., Park, J., Kaufmann, G. F., & Janda, K. D. (2008). An unexpected switch in the modulation of AI-2-based quorum sensing discovered through synthetic 4, 5-dihydroxy-2, 3-pentanedione analogues. Journal of the American Chemical Society, 130(29), 9200–9201.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Roy, V., Adams, B. L., & Bentley, W. E. (2011). Developing next generation antimicrobials by intercepting AI-2 mediated quorum sensing. Enzyme and Microbial Technology, 49(2), 113–123.PubMedCrossRefGoogle Scholar
  85. 85.
    Biswas, N. N., Kutty, S. K., Iskander, G. M., Mielczarek, M., Bhadbhade, M. M., Gardner, C. R., ..., Kumar, N. (2016). Synthesis of brominated novel N-heterocycles: New scaffolds for antimicrobial discovery. Tetrahedron, 72(4), 539–546.CrossRefGoogle Scholar
  86. 86.
    Li, G., Yan, C., Xu, Y., Feng, Y., Wu, Q., Lv, X., ..., Xia, X. (2014b). Punicalagin inhibits Salmonella virulence factors and has anti-quorum-sensing potential. Applied and environmental microbiology, 80(19), 6204–6211.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Huber, B., Eberl, L., Feucht, W., & Polster, J. (2003). Influence of polyphenols on bacterial biofilm formation and quorum-sensing. Zeitschrift für Naturforschung C, 58(11–12), 879–884.CrossRefGoogle Scholar
  88. 88.
    Bjarnsholt, T., Jensen, P. Ø., Rasmussen, T. B., Christophersen, L., Calum, H., Hentzer, M., ..., Høiby, N. (2005). Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology, 151(12), 3873–3880.PubMedCrossRefGoogle Scholar
  89. 89.
    Choo, J. H., Rukayadi, Y., & Hwang, J. K. (2006). Inhibition of bacterial quorum sensing by vanilla extract. Letters in Applied Microbiology, 42(6), 637–641.PubMedGoogle Scholar
  90. 90.
    Almasoud, A., Hettiarachchy, N., Rayaprolu, S., Babu, D., Kwon, Y. M., & Mauromoustakos, A. (2016). Inhibitory effects of lactic and malic organic acids on autoinducer type 2 (AI-2) quorum sensing of Escherichia coli O157: H7 and Salmonella typhimurium. LWT- Food Science and Technology, 66, 560–564.CrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesSunway UniversityPetaling JayaMalaysia

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