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Quorum sensing regulation in bacteria of the family enterobacteriaceae

  • Reviews and Theoretical Articles
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Abstract

Bacteria are able to sense an increase in population density and can respond to it by coordinated regulation of the expression of certain sets of genes in the total population of bacteria. This specific mode of regulation is known as Quorum Sensing (QS). The QS systems include low-molecular-weight signaling molecules of different chemical nature and the regulatory proteins that interact with the signaling molecules. The QS systems are global regulators of bacterial gene expression. They play an important role in controlling metabolic processes in bacteria. This review describes QS systems in members of the bacterial family Enterobacteriaceae functioning with the involvement of various signaling molecules, including N-acyl-homoserine lactones, AI-2, AI-3, peptides, and indole. The differences of the QS system in these bacteria from those in other taxonomic groups of bacteria are discussed. Data on the role of different types of QS systems in the regulation of different cellular processes in bacteria, i.e., their virulence, the synthesis of enzymes and antibiotics, biofilm formation, apoptosis, etc. are presented.

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References

  1. Fuqua, C., Winans, S.C., and Greenberg, E.P., Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators, Annu. Rev. Microbiol., 1996, vol. 50, pp. 727–751.

    Article  CAS  PubMed  Google Scholar 

  2. Miller, M.B. and Bassler, B.L., Quorum sensing in bacteria, Annu. Rev. Microbiol., 2001, vol. 55, pp. 165–199.

    Article  CAS  PubMed  Google Scholar 

  3. Waters, C.M. and Bassler, B.L., Quorum sensing: cell-to-cell communication in bacteria, Annu. Rev. Cell. Dev. Biol., 2005, vol. 21, pp. 319–346.

    Article  CAS  PubMed  Google Scholar 

  4. Khmel, I.A. and Metlitskaya, A.Z., Quorum sensing regulation of gene expression: a promising target for drugs against bacterial pathogenicity, Mol. Biol. (Moscow), 2006, vol. 40, pp. 195–210.

    Article  CAS  Google Scholar 

  5. Khmel, I.A., Quorum sensing regulation of gene expression: fundamental and applied aspects, the role in bacterial communication, Mikrobiologiya, 2006, vol. 75, pp. 457–464.

    CAS  Google Scholar 

  6. Van Houdt, R., Givskov, M., and Michiels, C.W., Quorum sensing in Serratia, FEMS Microbiol. Rev., 2007, vol. 31, pp. 407–424.

    Article  PubMed  CAS  Google Scholar 

  7. Atkinson, S. and Williams, P., Quorum sensing and social networking in the microbial world, J. R. Soc. Interface, 2009, vol. 6, pp. 959–978.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. De Kievit, T.R. and Iglewski, B.H., Bacterial quorum sensing in pathogenic relationships, Infect. Immun., 2000, vol. 68, pp. 4839–4849.

    Article  PubMed Central  PubMed  Google Scholar 

  9. Parsek, M.R. and Greenberg, E.P., Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 8789–8793.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Schauder, S. and Bassler, B.L., The languages of bacteria, Genes Dev., 2001, vol. 15, pp. 1468–1480.

    Article  CAS  PubMed  Google Scholar 

  11. Veselova, M., Kholmeckaya, M., Klein, S., et al., Production of N-acylhomoserine lactone signal molecules by gram-negative soil-borne and plant-associated bacteria, Folia Microbiol., 2003, vol. 48, pp. 794–798.

    Article  CAS  Google Scholar 

  12. Nasser, W., Bouillant, M.L., Salmond, G., and Reverchon, S., Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N-acylhomoserine lactone signal molecules, Mol. Microbiol., 1998, vol. 29, pp. 1391–1405.

    Article  CAS  PubMed  Google Scholar 

  13. Horng, Y.T., Deng, S.C., Daykin, M., et al., The LuxR family protein SpnR functions as a negative regulator of N-acylhomoserine lactone-dependent quorum sensing in Serratia marcescens, Mol. Microbiol., 2002, vol. 45, pp. 1655–1671.

    Article  CAS  PubMed  Google Scholar 

  14. Chatterjee, A., Cui, Y., Hasegawa, H., et al., Comparative analysis of two classes of quorum-sensing signalling systems that control production of extracellular proteins and secondary metabolites in Erwinia carotovora subspecies, J. Bacteriol., 2005, vol. 187, pp. 8026–8038.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Molina, L., Rezzonico, F., Defago, G., and Duffy, B., Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen, J. Bacteriol., 2005, vol. 187, pp. 3206–3213.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Liu, X., Jia, J., Popat, R., et al., Characterisation of two quorum sensing systems in the endophytic Serratia plymuthica strain G3: differential control of motility and biofilm formation according to life-style, BMC Microbiol., 2011, vol. 11, p. 26.

  17. Watson, W.T., Minogue, T.D., Val, D.L., et al., Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing, Mol. Cell, 2002, vol. 9, pp. 685–694.

    Article  CAS  PubMed  Google Scholar 

  18. Gould, T.A., Herman, J., Krank, J., et al., Specificity of acyl-homoserine lactone synthases examined by mass spectrometry, J. Bacteriol., 2006, vol. 188, pp. 773–783.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Devine, J.H., Shadel, G.S., and Baldwin, T.O., Identification of the ope tor of the lux regulon from the Vibrio fischeri strain ATCC7744, Proc. Natl. Acad. Sci. USA, 1989, vol. 86, pp. 5688–5692.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Finney, A.H., Blick, R.J., Murakami, K., et al., Role of the C-terminal domain of the alpha subunit of RNA polymerase in LuxR-dependent transcriptional activation of the lux operon during quorum sensing, J. Bacteriol., 2002, vol. 184, pp. 4520–4528.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Beck von Bodman, S. and Farrand, S.K., Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer, J. Bacteriol., 1995, vol. 177, pp. 5000–5008.

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Von Bodman, S.B., Majerczak, D.R., and Coplin, D.L., A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii, Proc. Natl Acad. Sci USA, 1998, vol. 95, pp. 7687–7692.

    Article  Google Scholar 

  23. Minogue, T.D., Wehland-von Trebra, M., Bernhard, F., and von Bodman, S.B., The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function, Mol. Microbiol., 2002, vol. 44, no. 6, pp. 1625–1635.

    Article  CAS  PubMed  Google Scholar 

  24. Castang, S., Reverchon, S., Gouet, P., and Nasser, W., Direct evidence for the modulation of the activity of the Erwinia chrysanthemi quorum-sensing regulator ExpR by acylhomoserine lactone pheromone, J. Biol. Chem., 2006, vol. 281, pp. 29972–29987.

    Article  CAS  PubMed  Google Scholar 

  25. Atkinson, S., Throup, J.P., Stewart, G.S., and Williams, P., A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping, Mol. Microbiol., 1999, vol. 33, pp. 1267–1277.

    Article  CAS  PubMed  Google Scholar 

  26. Atkinson, S., Chang, C.Y., Patrick, H.L., et al., Functional interplay between the Yersinia pseudotuberculosis YpsRI and YtbRI quorum sensing systems modulates swimming motility by controlling expression of flhDC and fliA, Mol. Microbiol., 2008, vol. 69, pp. 137–151.

    Article  CAS  PubMed  Google Scholar 

  27. Van Houdt, R., Moons, P., Aertsen, A., et al., 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., 2007, vol. 158, pp. 150–158.

    Article  PubMed  CAS  Google Scholar 

  28. Smith, J.N. and Ahmer, B.M., Detection of other microbial species by Salmonella: expression of the SdiA regulon, J. Bacteriol., 2003, vol. 185, pp. 1357–1366.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Sabag-Daigle, A. and Ahmer, B.M., ExpI and PhzI are descendants of the long lost cognate signal synthase for SdiA, PLoS One, 2012, vol. 7, e47720.

  30. Michael, B., Smith, J.N., Swift, S., et al., SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities, J. Bacteriol., 2001, vol. 183, pp. 5733–5742.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Yao, Y., Martinez-Yamout, M.A., Dickerson, T.J., et al., Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones, J. Mol. Biol., 2006, vol. 355, pp. 262–273.

    Article  CAS  PubMed  Google Scholar 

  32. Bainton, N.J., Stead, P., Chhabra, S.R., et al., N-(3-Oxohexanoyl)-l-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora, Biochem. J., 1992, vol. 288, pp. 997–1004.

    CAS  PubMed Central  PubMed  Google Scholar 

  33. McGowan, S., Sebaihia, M., Jones, S., et al., Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator, Microbiology, 1995, vol. 141, pp. 541–550.

    Article  CAS  PubMed  Google Scholar 

  34. McGowan, S.J., Sebaihia, M., O’Leary, S., et al., Analysis of the carbapenem gene cluster of Erwinia carotovora: definition of the antibiotic biosynthetic genes and evidence for a novel beta-lactam resistance mechanism, Mol. Microbiol., 1997, vol. 26, pp. 545–556.

    Article  CAS  PubMed  Google Scholar 

  35. Coulthurst, S.J., Barnard, A.M., and Salmond, G.P., Regulation and biosynthesis of carbapenem antibiotics in bacteria, Nat. Rev. Microbiol., 2005, vol. 3, pp. 295–306.

    Article  CAS  PubMed  Google Scholar 

  36. Welch, M., Todd, D.E., Whitehead, N.A., et al., N-Acylhomoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia, EMBO J., 2000, vol. 19, pp. 631–641.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Thomson, N.R., Crow, M.A., McGowan, S.J., et al., Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control, Mol. Microbiol., 2000, vol. 36, pp. 539–556.

    Article  CAS  PubMed  Google Scholar 

  38. Fineran, P.C., Slater, H., Everson, L., et al., Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production, Mol. Microbiol., 2005, vol. 56, pp. 1495–1517.

    Article  CAS  PubMed  Google Scholar 

  39. Slater, H., Crow, M., Everson, L., and Salmond, G.P., Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways, Mol. Microbiol., 2003, vol. 47, pp. 303–320.

    Article  CAS  PubMed  Google Scholar 

  40. Harris, A.K., Williamson, N.R., Slater, H., et al., The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and straindependent genome context variation, Microbiology, 2004, vol. 150, pp. 3547–3560.

    Article  CAS  PubMed  Google Scholar 

  41. Liu, X., Bimerew, M., Ma, Y., et al., Quorum-sensing signalling is required for production of the antibiotic pyrrolnitrin in a rhizospheric biocontrol strain of Serratia plymuthica, FEMS Microbiol. Lett., 2007, vol. 270, pp. 299–305.

    Article  CAS  PubMed  Google Scholar 

  42. Toth, I.K., Pritchard, L., and Birch, P.R., Comparative genomics reveals what makes an enterobacterial plant pathogen, Annu. Rev. Phytopathol., 2006, vol. 44, pp. 305–336.

    Article  CAS  PubMed  Google Scholar 

  43. Jones, S., Yu, B., Bainton, N.J., et al., The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa, EMBO J., 1993, vol. 12, pp. 2477–2482.

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Pirhonen, M., Flego, D., Heikinheimo, R., and Palva, E.T., A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora, EMBO J., 1993, vol. 12, pp. 2467–2476.

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Sjoblom, S., Brader, G., Koch, G., and Palva, E.T., Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora, Mol. Microbiol., 2006, vol. 60, pp. 1474–1489.

    Article  CAS  PubMed  Google Scholar 

  46. Cui, Y., Chatterjee, A., Hasegawa, H., et al., ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein, J. Bacteriol., 2005, vol. 187, pp. 4792–4803.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Chatterjee, A., Cui, Y., Hasegawa, H., et al., Comparative analysis of two classes of quorum-sensing signaling systems that control production of extracellular proteins and secondary metabolites in Erwinia carotovora subspecies, J. Bacteriol., 2005, vol. 187, pp. 8026–8038.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Riedel, K., Ohnesorg, T., Krogfelt, K.A., et al., N-Acyl-L-homoserine lactone-mediated regulation of the lip secretion system in Serratia liquefaciens MG1, J. Bacteriol., 2001, vol. 183, pp. 1805–1809.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Christensen, A.B., Riedel, K., Eberl, L., et al., Quorum-sensing-directed protein expression in Serratia proteamaculans B5a, Microbiology, 2003, vol. 149, pp. 471–483.

    Article  CAS  PubMed  Google Scholar 

  50. Coulthurst, S.J., Williamson, N.R., Harris, A.K., et al., Metabolic and regulatory engineering of Serratia marcescens: mimicking phage-mediated horizontal acquisition of antibiotic biosynthesis and quorumsensing capacities, Microbiology, 2006, vol. 152, pp. 1899–1911.

    Article  CAS  PubMed  Google Scholar 

  51. Henrichsen, J., Bacterial surface translocation: a survey and a classification, Bacteriol. Rev., 1972, vol. 36, pp. 478–503.

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Eberl, L., Molin, S., and Givskov, M., Surface motility of Serratia liquefaciens MG1, J. Bacteriol., 1999, vol. 181, pp. 1703–1712.

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Fraser, G.M. and Hughes, C., Swarming motility, Curr. Opin. Microbiol., 1999, vol. 2, pp. 630–635.

    Article  CAS  PubMed  Google Scholar 

  54. Daniels, R., Vanderleyden, J., and Michiels, J., Quorum sensing and swarming migration in bacteria, FEMS Microbiol. Rev., 2004, vol. 28, pp. 261–289.

    Article  CAS  PubMed  Google Scholar 

  55. Eberl, L., Winson, M.K., Sternberg, C., et al., Involvement of N-acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens, Mol. Microbiol., 1996, vol. 20, pp. 127–136.

    Article  CAS  PubMed  Google Scholar 

  56. Lindum, P.W., Anthoni, U., Christophersen, C., et al., N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1, J. Bacteriol., 1998, vol. 180, pp. 6384–6388.

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Dong, Y.H., Wang, L.H., Xu, J.L., et al., Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase, Nature, 2001, vol. 411, pp. 813–817.

    Article  CAS  PubMed  Google Scholar 

  58. Muller, H., Westendorf, C., Leitner, E., et al., Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48, FEMS Microbiol. Ecol., 2009, vol. 67, pp. 468–478.

    Article  PubMed  CAS  Google Scholar 

  59. Atkinson, S., Chang, C.Y., Sockett, R.E., et al., Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility, J. Bacteriol., 2006, vol. 188, pp. 1451–1461.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Hussain, M.B., Zhang, H.B., Xu, J.L., et al., The acylhomoserine lactone-type quorum-sensing system modulates cell motility and virulence of Erwinia chrysanthemi pv. zeae, J. Bacteriol., 2008, vol. 190, pp. 1045–1053.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Allison, C., Emody, L., Coleman, N., and Hughes, C., The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis, J. Infect. Dis., 1994, vol. 169, pp. 1155–1158.

    Article  CAS  PubMed  Google Scholar 

  62. Costerton, J.W., Lewandowski, Z., Caldwell, D.E., et al., Microbial biofilms, Annu. Rev. Microbiol., 1995, vol. 49, pp. 711–745.

    Article  CAS  PubMed  Google Scholar 

  63. Ilyina, T.S., Romanova, Yu.M., and Gintsburg, A.L., Biofilms as a mode of existence of bacteria in external environment and host body: the phenomenon, genetic control, and regulation systems of development, Russ. J. Genet., 2004, vol. 40, no. 11, pp. 1089–1098.

    Article  Google Scholar 

  64. Costerton, J.W., Stewart, P.S., and Greenberg, E.P., Bacterial biofilms: a common cause of persistent infections, Science, 1999, vol. 284, pp. 1318–1322.

    Article  CAS  PubMed  Google Scholar 

  65. Davies, D.G., Parsek, M.R., Pearson, J.P., et al., The involvement of cell-to-cell signals in the development of a bacterial biofilm, Science, 1998, vol. 280, pp. 295–298.

    Article  CAS  PubMed  Google Scholar 

  66. Labbate, M., Zhu, H., Thung, L., et al., Quorumsensing regulation of adhesion in Serratia marcescens MG1 is surface dependent, J. Bacteriol., 2007, vol. 189, pp. 2702–2711.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Rice, S.A., Koh, K.S., Queck, S.Y., et al., Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues, J. Bacteriol., 2005, vol. 187, pp. 3477–3485.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Labbate, M., Queck, S.Y., Koh, K.S., et al., Quorum sensing-controlled biofilm development in Serratia liquefaciens MG1, J. Bacteriol., 2004, vol. 186, pp. 692–698.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Moons, P., Van Houdt, R., Aertsen, A., et al., Role of quorum sensing and antimicrobial component production by Serratia plymuthica in formation of biofilms, including mixed biofilms with Escherichia coli, Appl. Environ. Microbiol., 2006, vol. 72, pp. 7294–7300.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Zaitseva, Yu.V., Voloshina, P.V., Liu, Kh., et al., Involvement of the global regulators GrrS, RpoS, and SplIR in formation of biofilms in Serratia plymuthica, Russ. J. Genet., 2010, vol. 46, no. 5, pp. 541–545.

    Article  CAS  Google Scholar 

  71. Viana, E.S., Campos, M.E., Ponce, A.R., et al., Biofilm formation and acyl homoserine lactone production in Hafnia alvei isolated from raw milk, Biol. Res., 2009, vol. 42, pp. 427–436.

    CAS  PubMed  Google Scholar 

  72. Koutsoudis, M.D., Tsaltas, D., Minogue, T.D., and von Bodman, S.B., Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 5983–5988.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Atkinson, S., Sockett, R.E., Camara, M., and Williams, P., Quorum sensing and the lifestyle of Yersinia, Curr. Issues Mol. Biol., 2006, vol. 8, pp. 1–10.

    CAS  PubMed  Google Scholar 

  74. Bobrov, A.G., Bearden, S.W., Fetherston, J.D., et al., Functional quorum sensing systems affect biofilm formation and protein expression in Yersinia pestis, Adv. Exp. Med. Biol., 2007, vol. 603, pp. 178–191.

    Article  PubMed  Google Scholar 

  75. Lee, J., Jayaraman, A., and Wood, T.K., Indole is an inter-species biofilm signal mediated by SdiA, BMC Microbiol., 2007, vol. 7, p. 42.

  76. Toth, I.K., Bell, K.S., Holeva, M.C., and Birch, P.R., Soft rot erwiniae: from genes to genomes, Mol. Plant Pathol., 2003, vol. 4, pp. 17–30.

    Article  CAS  PubMed  Google Scholar 

  77. Smadja, B., Latour, X., Faure, D., et al., Involvement of N-acylhomoserine lactones throughout plant infection by Erwinia carotovora subsp. atroseptica (Pectobacterium atrosepticum), Mol. Plant-Microbe Interact., 2004, vol. 17, pp. 1269–1278.

    Article  CAS  PubMed  Google Scholar 

  78. Pemberton, C.L., Whitehead, N.A., Sebaihia, M., et al., Novel quorum-sensing-controlled genes in Erwinia carotovora subsp. carotovora: identification of a fungal elicitor homologue in a soft-rotting bacterium, Mol. Plant-Microbe Interact., 2005, vol. 18, pp. 343–353.

    Article  CAS  PubMed  Google Scholar 

  79. Corbett, M., Virtue, S., Bell, K., et al., Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway, Mol. Plant-Microbe Interact., 2005, vol. 18, pp. 334–342.

    Article  CAS  PubMed  Google Scholar 

  80. Burr, T., Barnard, A.M., Corbett, M.J., et al., Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor, Mol. Microbiol., 2006, vol. 59, pp. 113–125.

    Article  CAS  PubMed  Google Scholar 

  81. Cui, Y., Chatterjee, A., Hasegawa, H., and Chatterjee, A.K., Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals, J. Bacteriol., 2006, vol. 188, pp. 4715–4726.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Bell, K.S., Sebaihia, M., Pritchard, L., et al., Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 11105–11110.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Minogue, T.D., Carlier, A.L., Koutsoudis, M.D., and von Bodman, S.B., The cell density-dependent expression of stewartan exopolysaccharide in Pantoea stewartii ssp. stewartii is a function of EsaR-mediated repression of the rcsA gene, Mol. Microbiol., 2005, vol. 56, pp. 189–203.

    Article  CAS  PubMed  Google Scholar 

  84. Chen, Z., Li, B., Zhang, J., et al., Quorum sensing affects virulence-associated proteins F1, LcrV, KatY and pH6 etc. of Yersinia pestis as revealed by protein microarray-based antibody profiling, Microbes Infect., 2006, vol. 8, pp. 2501–2508.

    Article  CAS  PubMed  Google Scholar 

  85. Gelhaus, H.C., Rozak, D.A., Nierman, W.C., et al., Exogenous Yersinia pestis quorum sensing molecules N-octanoyl-homoserine lactone and N-(3-oxooctanoyl)-homoserine lactone regulate the LcrV virulence factor, Microb. Pathol., 2009, vol. 46, pp. 283–287.

    Article  CAS  Google Scholar 

  86. Ahmer, B.M., van Reeuwijk, J., Timmers, C.D., et al., Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid, J. Bacteriol., 1998, vol. 180, pp. 1185–1193.

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Dyszel, J.L., Smith, J.N., Lucas, D.E., et al., Salmonella enterica serovar Typhimurium can detect acyl homoserine lactone production by Yersinia enterocolitica in mice, J. Bacteriol., 2010, vol. 192, pp. 29–37.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  88. Frankel, G., Phillips, A.D., Rosenshine, I., et al., Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements, Mol. Microbiol., 1998, vol. 30, pp. 911–921.

    Article  CAS  PubMed  Google Scholar 

  89. Law, D., Virulence factors of Escherichia coli O157 and other Shiga toxin-producing E. coli, J. Appl. Microbiol., 2000, vol. 88, pp. 729–745.

    Article  CAS  PubMed  Google Scholar 

  90. Kanamaru, K., Kanamaru, K., Tatsuno, I., et al., SdiA, an Escherichia coli homologue of quorum-sensing regulators, controls the expression of virulence factors in enterohaemorrhagic Escherichia coli O157:H7, Mol. Microbiol., 2000, vol. 38, pp. 805–816.

    Article  CAS  PubMed  Google Scholar 

  91. Dziva, F., van Diemen, P.M., Stevens, M.P., et al., Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis, Microbiology, 2004, vol. 150, pp. 3631–3645.

    Article  CAS  PubMed  Google Scholar 

  92. Sharma, V.K., Bearson, S.M., and Bearson, B.L., Evaluation of the effects of SdiA, a LuxR homologue, on adherence and motility of Escherichia coli O157:H7, Microbiology, 2010, vol. 156, pp. 1303–1312.

    Article  CAS  PubMed  Google Scholar 

  93. Hughes, D.T., Terekhova, D.A., Liou, L., et al., Chemical sensing in mammalian host-bacterial commensal associations, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 9831–9836.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  94. Van Houdt, R., Moons, P., Hueso Buj, M., and Michiels, C.W., N-Acyl-L-homoserine lactone quorum sensing controls butanediol fermentation in Serratia plymuthica RVH1 and Serratia marcescens MG1, J. Bacteriol., 2006, vol. 188, pp. 4570–4572.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  95. Moons, P., Van Houdt, R., Vivijs, B., et al., Integrated regulation of acetoin fermentation by quorum sensing and pH in Serratia plymuthica RVH1, Appl. Environ. Microbiol., 2011, vol. 77, pp. 3422–3427.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  96. Bassler, B.L., Wright, M., and Silverman, M.R., Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway, Mol. Microbiol., 1994, vol. 13, pp. 273–286.

    Article  CAS  PubMed  Google Scholar 

  97. Miller, S.T., Xavier, K.B., Campagna, S.R., et al., Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2, Mol. Cell, 2004, vol. 15, pp. 677–687.

    Article  CAS  PubMed  Google Scholar 

  98. Xavier, K.B. and Bassler, B.L., Interference with AI-2-mediated bacterial cell-cell communication, Nature, 2005, vol. 437, pp. 750–753.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  99. Surette, M.G. and Bassler, B.L., Quorum sensing in Escherichia coli and Salmonella typhimurium, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 7046–7050.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  100. Surette, M.G., Miller, M.B., and Bassler, B.L., Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 1639–1644.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  101. Taga, M.E., Miller, S.T., and Bassler, B.L., Lsr-Mediated transport and processing of AI-2 in Salmonella typhimurium, Mol. Microbiol., 2003, vol. 50, pp. 1411–1427.

    Article  CAS  PubMed  Google Scholar 

  102. Xavier, K.B. and Bassler, B.L., Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli, J. Bacteriol., 2005, vol. 187, pp. 238–248.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  103. Sperandio, V., Mellies, J.L., Nguyen, W., et al., Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 15196–15201.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  104. Gonzalez Barrios, A.F., Zuo, R., Hashimoto, Y., et al., Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022), J. Bacteriol., 2006, vol. 188, pp. 305–316.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  105. DeLisa, M.P., Wu, C.F., Wang, L., et al., DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli, J. Bacteriol., 2001, vol. 183, pp. 5239–5247.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  106. Sperandio, V., Torres, A.G., Giron, J.A., and Kaper, J.B., Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7, J. Bacteriol., 2001, vol. 183, pp. 5187–5197.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  107. Coulthurst, S.J., Kurz, C.L., and Salmond, G.P., luxS mutants of Serratia defective in autoinducer-2-dependent’ quorum sensing’ show strain-dependent impacts on virulence and production of carbapenem and prodigiosin, Microbiology, 2004, vol. 150, pp. 1901–1910.

    Article  CAS  PubMed  Google Scholar 

  108. Coulthurst, S.J., Lilley, K.S., and Salmond, G.P., Genetic and proteomic analysis of the role of luxS in the enteric phytopathogen, Erwinia carotovora, Mol. Plant Pathol., 2006, vol. 7, pp. 31–45.

    Article  CAS  PubMed  Google Scholar 

  109. Gao, Y., Song, J., Hu, B., et al., The luxS gene is involved in AI-2 production, pathogenicity, and some phenotypes in Erwinia amylovora, Curr. Microbiol., 2009, vol. 58, pp. 1–10.

    Article  CAS  PubMed  Google Scholar 

  110. Schauder, S., Shokat, K., Surette, M.G., and Bassler, B.L., The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule, Mol. Microbiol., 2001, vol. 41, pp. 463–476.

    Article  CAS  PubMed  Google Scholar 

  111. Taga, M.E., Semmelhack, J.L., and Bassler, B.L., The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium, Mol. Microbiol., 2001, vol. 42, pp. 777–793.

    Article  CAS  PubMed  Google Scholar 

  112. Rezzonico, F. and Duffy, B., Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria, BMC Microbiol., 2008, vol. 8, p. 154.

  113. Sperandio, V., Torres, A.G., Jarvis, B., et al., Bacteria-host communication: the language of hormones, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 8951–8956.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  114. Walters, M. and Sperandio, V., Quorum sensing in Escherichia coli and Salmonella, Int. J. Med. Microbiol., 2006, vol. 296, pp. 125–131.

    Article  CAS  PubMed  Google Scholar 

  115. Shpakov, A.O., QS-Type bacterial signal molecules of nonpeptide origin, Mikrobiologiya, 2009, vol. 78, pp. 163–175.

    CAS  Google Scholar 

  116. Walters, M., Sircili, M.P., and Sperandio, V., AI-3 synthesis is not dependent on luxS in Escherichia coli, J. Bacteriol., 2006, vol. 188, pp. 5668–5681.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  117. Gospodarek, E., Bogiel, T., and Zalas-Wiecek, P., Communication between microorganisms as a basis for production of virulence factors, Pol. J. Microbiol., 2009, vol. 58, pp. 191–198.

    CAS  PubMed  Google Scholar 

  118. Sperandio, V., Torres, A.G., and Kaper, J.B., Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli, Mol. Microbiol., 2002, vol. 43, pp. 809–821.

    Article  CAS  PubMed  Google Scholar 

  119. Clarke, M.B., Hughes, D.T., Zhu, C., et al., The QseC sensor kinase: a bacterial adrenergic receptor, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 10420–10425.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  120. Habdas, B.J., Smart, J., Kaper, J.B., and Sperandio, V., The LysR-type transcriptional regulator QseD alters type three secretion in enterohemorrhagic Escherichia coli and motility in K-12 Escherichia coli, J. Bacteriol., 2010, vol. 192, pp. 3699–3712.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  121. Burton, C.L., Chhabra, S.R., Swift, S., et al., The growth response of Escherichia coli to neurotransmitters and related catecholamine drugs requires a functional enterobactin biosynthesis and uptake system, Infect. Immun., 2002, vol. 70, pp. 5913–5923.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  122. Lyte, M., Arulanandam, B.P., and Frank, C.D., Production of Shiga-like toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine, J. Lab. Clin. Med., 1996, vol. 128, pp. 392–398.

    Article  CAS  PubMed  Google Scholar 

  123. Kendall, M.M., Rasko, D.A., and Sperandio, V., Global effects of the cell-to-cell signaling molecules autoinducer-2, autoinducer-3, and epinephrine in a luxS mutant of enterohemorrhagic Escherichia coli, Infect. Immun., 2007, vol. 75, pp. 4875–4884.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  124. Lewis, K., Programmed death in bacteria, Microbiol. Mol. Biol. Rev., 2000, vol. 64, pp. 503–514.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  125. Samuilov, V.D., Oleskin, A.V., and Lagunova, E.M., Programmed cell death, Biochemistry (Moscow), 2000, vol. 65, pp. 1029–1046.

    Google Scholar 

  126. Yamaguchi, Y., Park, J.H., and Inouye, M., Toxinantitoxin systems in bacteria and archaea, Ann. Rev. Genet., 2011, vol. 45, pp. 61–79.

    Article  CAS  PubMed  Google Scholar 

  127. Mittenhuber, G., Occurrence of mazEF-like antitoxin/toxin systems in bacteria, J. Mol. Microbiol. Biotechnol., 1999, vol. 1, pp. 295–302.

    CAS  PubMed  Google Scholar 

  128. Hayes, F., Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest, Science, 2003, vol. 301, pp. 1496–1499.

    Article  CAS  PubMed  Google Scholar 

  129. Aizenman, E., Engelberg-Kulka, H., and Glaser, G., An Escherichia coli chromosomal “addiction module” regulated by guanosine [corrected] 3’,5’-bispyrophosphate: a model for programmed bacterial cell death, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 6059–6063.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  130. Engelberg-Kulka, H., Hazan, R., and Amitai, S., mazEF: a chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria, J. Cell Sci., 2005, vol. 118, pp. 4327–4332.

    Article  CAS  PubMed  Google Scholar 

  131. Zhang, Y., Zhang, J., Hoeflich, K.P., et al., MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli, Mol. Cell, 2003, vol. 12, pp. 913–923.

    Article  CAS  PubMed  Google Scholar 

  132. Zhang, Y., Zhang, J., Hara, H., et al., Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase, J. Biol. Chem., 2005, vol. 280, pp. 3143–3150.

    Article  CAS  PubMed  Google Scholar 

  133. Hazan, R., Sat, B., and Engelberg-Kulka, H., Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions, J. Bacteriol., 2004, vol. 186, pp. 3663–3669.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  134. Kumar, S., Kolodkin-Gal, I., and Engelberg-Kulka, H., Novel quorum-sensing peptides mediating interspecies bacterial cell death, MBio., 2013, vol. 4. doi: 10.1128/mBio.00314-13

  135. Kolodkin-Gal, I., Hazan, R., Gaathon, A., et al., A linear pentapeptide is a quorum-sensing factor required for mazEF-mediated cell death in Escherichia coli, Science, 2007, vol. 318, pp. 652–655.

    Article  CAS  PubMed  Google Scholar 

  136. Kolodkin-Gal, I. and Engelberg-Kulka, H., The extracellular death factor: physiological and genetic factors influencing its production and response in Escherichia coli, J. Bacteriol., 2008, vol. 190, pp. 3169–3175.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  137. Belitsky, M., Avshalom, H., Erental, A., et al., The Escherichia coli extracellular death factor EDF induces the endoribonucleolytic activities of the toxins MazF and ChpBK, Mol. Cell, 2011, vol. 41, pp. 625–635.

    Article  CAS  PubMed  Google Scholar 

  138. Wang, D., Ding, X., and Rather, P.N., Indole can act as an extracellular signal in Escherichia coli, J. Bacteriol., 2001, vol. 183, pp. 4210–4216.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  139. Ahmer, B.M., Cell-to-cell signalling in Escherichia coli and Salmonella enterica, Mol. Microbiol., 2004, vol. 52, pp. 933–945.

    Article  CAS  PubMed  Google Scholar 

  140. Hirakawa, H., Inazumi, Y., Masaki, T., et al., Indole induces the expression of multidrug exporter genes in Escherichia coli, Mol. Microbiol., 2005, vol. 55, pp. 1113–1126.

    Article  CAS  PubMed  Google Scholar 

  141. Anyanful, A., Dolan-Livengood, J.M., Lewis, T., et al., Paralysis and killing of Caenorhabditis elegans by enteropathogenic Escherichia coli requires the bacterial tryptophanase gene, Mol. Microbiol., 2005, vol. 57, pp. 988–1007.

    Article  CAS  PubMed  Google Scholar 

  142. Chant, E.L. and Summers, D.K., Indole signaling contributes to the stable maintenance of Escherichia coli multicopy plasmids, Mol. Microbiol., 2007, vol. 63, pp. 35–43.

    Article  CAS  PubMed  Google Scholar 

  143. Sabag-Daigle, A., Soares, J.A., Smith, J.N., et al., The acyl homoserine lactone receptor, SdiA, of Escherichia coli and Salmonella enterica serovar Typhimurium does not respond to indole, Appl. Environ. Microbiol., 2012, vol. 78, pp. 5424–5431.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  144. Andersson, R.A., Eriksson, A.R., Heikinheimo, R., et al., Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expR(Ecc), Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 384–393.

    Article  CAS  PubMed  Google Scholar 

  145. Gray, K.M. and Garey, J.R., The evolution of bacterial LuxI and LuxR quorum sensing regulators, Microbiology, 2001, vol. 147, pp. 2379–2387.

    CAS  PubMed  Google Scholar 

  146. Wei, J.-R., Tsai, Y.-H., Horng, Y.-T., et al., A mobile quorum-sensing system in Serratia marcescens, J. Bacteriol., 2006, vol. 188, pp. 1518–1525.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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  1. Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, 123182, Russia

    Yu. V. Zaitseva, A. A. Popova & I. A. Khmel

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Original Russian Text © Yu.V. Zaitseva, A.A. Popova, I.A. Khmel, 2014, published in Genetika, 2014, Vol. 50, No. 4, pp. 373–391.

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Zaitseva, Y.V., Popova, A.A. & Khmel, I.A. Quorum sensing regulation in bacteria of the family enterobacteriaceae. Russ J Genet 50, 323–340 (2014). https://doi.org/10.1134/S1022795414030120

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