1887

Abstract

Many bacteria use cell–cell communication mediated by diffusible signal molecules to monitor their population density or confinement to niches and to modulate their behaviour in response to these aspects of their environment. Work on signalling systems within individual species has formed a platform for studies of interspecies interactions that can occur within polymicrobial communities in nature. In addition to signalling between organisms that synthesize the same or related signal molecules, it is becoming evident that bacteria can sense signal molecules that they do not synthesize, thereby eavesdropping on signalling by other organisms in their immediate environment. Furthermore, molecules such as antibiotics that are considered not to be signals for the producing species can have effects on gene expression in other bacteria that indicate a signalling function. Interspecies signalling can lead to alteration in factors contributing to the virulence or persistence of bacterial pathogens as well as influencing the development of beneficial microbial communities. Here we review our current understanding of interspecies signalling in bacteria and the signals involved, what is known of the underlying signal transduction mechanisms and their influences on bacterial behaviour.

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2008-07-01
2024-03-28
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References

  1. Ahmer B. M. M. 2004; Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 52:933–945
    [Google Scholar]
  2. Ahmer B. M. 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. J Bacteriol 180:1185–1193
    [Google Scholar]
  3. Ansaldi M., Marolt D., Stebe T., Mandic-Mulec I., Dubnau D. 2002; Specific activation of the Bacillus quorum-sensing systems by isoprenylated pheromone variants. Mol Microbiol 44:1561–1573
    [Google Scholar]
  4. Anyanful A., Dolan-Livengood J. M., Lewis T., Sheth S., DeZalia M. N., Sherman M. A., Kalman L. V., Benian G. M., Kalman D. 2005; Paralysis and killing of Caenorhabditis elegans by enteropathogenic Escherichia coli requires the bacterial tryptophanase gene. Mol Microbiol 57:988–1007
    [Google Scholar]
  5. Baca-DeLancey R. R., South M. M. T., Ding X. D., Rather P. N. 1999; Escherichia coli genes regulated by cell-to-cell signaling. Proc Natl Acad Sci U S A 96:4610–4614
    [Google Scholar]
  6. Baltz R. H. 2007; Antimicrobials from Actinomycetes: back to the future. Am Soc Microbiol 2:125–131
    [Google Scholar]
  7. Barber C. E., Tang J. L., Feng J. X., Pan M. Q., Wilson T. J. G., Slater H., Dow J. M., Williams P., Daniels M. J. 1997; A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24:555–566
    [Google Scholar]
  8. Bassler B. L., Greenberg E. P., Stevens A. M. 1997; Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J Bacteriol 179:4043–4045
    [Google Scholar]
  9. Boon C., Deng Y., Wang L. H., He Y., Xu J. L., Fan Y., Pan S. Q., Zhang L. H. 2008; A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2:27–36
    [Google Scholar]
  10. Brazas M. D., Hancock R. E. W. 2005; Using microarray gene signatures to elucidate mechanisms of antibiotic action and resistance. Drug Discov Today 10:1245–1252
    [Google Scholar]
  11. Chater K. F., Horinouchi S. 2003; Signalling early developmental events in two highly diverged Streptomyces species. Mol Microbiol 48:9–15
    [Google Scholar]
  12. Chatterjee S., Wistrom C., Lindow S. E. 2008; A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proc Natl Acad Sci U S A 105:2670–2675
    [Google Scholar]
  13. 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 415:545–549
    [Google Scholar]
  14. Chun W., Cui J., Poplawsky A. 1997; Purification, characterization and biological role of a pheromone produced by Xanthomonas campestris pv. campestris. Physiol Mol Plant Pathol 51:1–14
    [Google Scholar]
  15. Clewell D. B., Francia M. V., Flannagan S. E., An F. Y. 2002; Enterococcal plasmid transfer: sex pheromones, transfer origins, relaxases, and the Staphylococcus aureus issue. Plasmid 48:193–201
    [Google Scholar]
  16. Colnaghi Simionato A. V., da Silva D. S., Lambais M. R., Carrilho E. 2007; Characterization of a putative Xylella fastidiosa diffusible signal factor by HRGC-EI-MS. J Mass Spectrom 42:1375–1381
    [Google Scholar]
  17. Davies J. 1990; What are antibiotics? Archaic functions for modern activities. Mol Microbiol 4:1227–1232
    [Google Scholar]
  18. Davies J. 2007; Microbes have the last word. EMBO Rep 8:616–621
    [Google Scholar]
  19. Davies J., Spiegelman G. B., Yim G. 2006; The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9:445–453
    [Google Scholar]
  20. Degrassi G., Aguilar C., Bosco M., Zahariev S., Pongor S., Venturi V. 2002; Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: cross-talk with quorum sensing bacterial sensors. Curr Microbiol 45:250–254
    [Google Scholar]
  21. DeLisa M. P., Wu C. F., Wang L., Valdes J. J., Bentley W. E. 2001; DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 183:5239–5247
    [Google Scholar]
  22. Diggle S. P., Cornelis P., Williams P., Cámara M. 2006; 4-Quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 296:83–91
    [Google Scholar]
  23. Domergue R., Castano I., De las Penas A., Zupancic M., Lockatell V., Hebel J. R., Johnson D., Cormack B. P. 2005; Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308:866–870
    [Google Scholar]
  24. Domka J., Lee J., Wood T. K. 2006; YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl Environ Microbiol 72:2449–2459
    [Google Scholar]
  25. Dong Y. H., Xu J. L., Li X. Z., Zhang L. H. 2000; AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci U S A 97:3526–3531
    [Google Scholar]
  26. Dong Y. H., Wang L. H., Xu J. L., Zhang H. B., Zhang X. F., Zhang L. H. 2001; Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–817
    [Google Scholar]
  27. Dow J. M., Crossman L., Findlay K., He Y. Q., Feng J. X., Tang J. L. 2003; Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A 100:10995–11000
    [Google Scholar]
  28. Duan K. M., Dammel C., Stein J., Rabin H., Surette M. G. 2003; Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50:1477–1491
    [Google Scholar]
  29. Dufour P., Jarraud S., Vandenesch F., Greenland T., Novick R. P., Bes M., Etienne J., Lina G. 2002; High genetic variability of the agr locus in Staphylococcus species. J Bacteriol 184:1180–1186
    [Google Scholar]
  30. Eberl L. 1999; N-Acyl homoserinelactone-mediated gene regulation in gram-negative bacteria. Syst Appl Microbiol 22:493–506
    [Google Scholar]
  31. Ferluga S., Bigirimana J., Höfte M., Venturi V. 2007; A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol Plant Pathol 8:529–538
    [Google Scholar]
  32. Fong K. P., Chung W. S. O., Lamont R. J., Demuth D. R. 2001; Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect Immun 69:7625–7634
    [Google Scholar]
  33. Fouhy Y., Scanlon K., Schouest K., Spillane C., Crossman L., Avison M. B., Ryan R. P., Dow J. M. 2007; Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia. J Bacteriol 189:4964–4968
    [Google Scholar]
  34. Gallio M., Sturgill G., Rather P., Kylsten P. 2002; A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes. Proc Natl Acad Sci U S A 99:12208–12213
    [Google Scholar]
  35. Goh E. B., Yim G., Tsui W., McClure J., Surette M. G., Davies J. 2002; Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc Natl Acad Sci U S A 99:17025–17030
    [Google Scholar]
  36. Haas W., Shepard B. D., Gilmore M. S. 2002; Two-component regulator of Enterococcus faecalis cytolysin responds to quorum-sensing autoinduction. Nature 415:84–87
    [Google Scholar]
  37. Hamoen L. W., Venema G., Kuipers O. P. 2003; Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology 149:9–17
    [Google Scholar]
  38. Havarstein L. S., Coomaraswamy G., Morrison D. A. 1995; An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc Natl Acad Sci U S A 92:11140–11144
    [Google Scholar]
  39. Higgins D. A., Pomianek M. E., Kraml C. M., Taylor R. K., Semmelhack M. F., Bassler B. L. 2007; The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883–886
    [Google Scholar]
  40. Hirakawa H., Inazumi Y., Masaki T., Hirata T., Yamaguchi A. 2005; Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55:1113–1126
    [Google Scholar]
  41. Hoffman L. R., D'Argenio D. A., MacCoss M. J., Zhang Z. Y., Jones R. A., Miller S. I. 2005; Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171–1175
    [Google Scholar]
  42. Holden M. T., Ram Chhabra S., de Nys R., Stead P., Bainton N. J., Hill P. J., Manefield M., Kumar N., Labatte M. other authors 1999; Quorum-sensing crosstalk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol Microbiol 33:1254–1266
    [Google Scholar]
  43. Holden M., Swift S., Williams P. 2000; New signal molecules on the quorum-sensing block. Trends Microbiol 8:101–104
    [Google Scholar]
  44. Horinouchi S. 1999 γ-Butyrolactones that Control Secondary Metabolism and Cell Differentiation in Streptomyces Washington, DC: American Society for Microbiology;
  45. Huang T. P., Wong A. C. L. 2007a; A cyclic AMP receptor protein-regulated cell-cell communication system mediates expression of a FecA homologue in Stenotrophomonas maltophilia. Appl Environ Microbiol 73:5034–5040
    [Google Scholar]
  46. Huang T. P., Wong A. C. L. 2007b; Extracellular fatty acids facilitate flagella-independent translocation by Stenotrophomonas maltophilia. Res Microbiol 158:702–711
    [Google Scholar]
  47. Hughes D. T., Sperandio V. 2008; Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111–120
    [Google Scholar]
  48. Jarraud S., Lyon G. J., Figueiredo A. M. S., Gerard L., Vandenesch F., Etienne J., Muir T. W., Novick R. P. 2000; Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J Bacteriol 182:6517–6522
    [Google Scholar]
  49. Jensen J. B., Egsgaard H., Vanonckelen H., Jochimsen B. U. 1995; Catabolism of indole-3-acetic-acid and 4-chloroindole-3-acetic and 5-chloroindole-3-acetic acid in Bradyrhizobium japonicum. J Bacteriol 177:5762–5766
    [Google Scholar]
  50. Ji G., Beavis R. C., Novick R. P. 1995; Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc Natl Acad Sci U S A 92:12055–12059
    [Google Scholar]
  51. Kanamaru K., Kanamaru K., Tatsuno I., Tobe T., Sasakawa C. 2000; SdiA, an Escherichia coli homologue of quorum-sensing regulators, controls the expression of virulence factors in enterohaemorrhagic Escherichia coli O157 : H7. Mol Microbiol 38:805–816
    [Google Scholar]
  52. Kato J. Y., Funa N., Watanabe H., Ohnishi Y., Horinouchi S. 2007; Biosynthesis of gamma-butyrolactone autoregulators that switch on secondary metabolism and morphological development in Streptomyces. Proc Natl Acad Sci U S A 104:2378–2383
    [Google Scholar]
  53. Konaklieva M. I., Plotkin B. J. 2006; Antimicrobial properties of organosulfur anti-infectives: a review of patent literature 1999–2005. Recent Patents Anti-Infect Drug Disc 1:177–180
    [Google Scholar]
  54. Labbate M., Queck S. Y., Koh K. S., Rice S. A., Givskov M., Kjelleberg S. 2004; Quorum sensing controlled biofilm development in Serratia liquefaciens MG1. J Bacteriol 186:692–698
    [Google Scholar]
  55. Lazazzera B. A., Grossman A. D. 1998; The ins and outs of peptide signaling. Trends Microbiol 6:288–294
    [Google Scholar]
  56. Lee S. W., Han S. W., Bartley L. E., Ronald P. C. 2006; Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proc Natl Acad Sci U S A 103:18395–18400
    [Google Scholar]
  57. Lee J., Bansal T., Jayaraman A., Bentley W. E., Wood T. K. 2007a; Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microbiol 73:4100–4109
    [Google Scholar]
  58. Lee J., Jayaraman A., Wood T. K. 2007b; Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7:42
    [Google Scholar]
  59. Lee S.-W., Jeong K.-S., Han S.-W., Lee S.-E., Phee B.-K., Hahn T.-R., Ronald P. 2008; The Xanthomonas oryzae pv. oryzae PhoP/Q two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J Bacteriol 190:2183–2197
    [Google Scholar]
  60. Lin J. T., Connelly M. B., Amolo C., Otani S., Yaver D. S. 2005; Global transcriptional response of Bacillus subtilis to treatment with subinhibitory concentrations of antibiotics that inhibit protein synthesis. Antimicrob Agents Chemother 49:1915–1926
    [Google Scholar]
  61. Linares J. F., Gustafsson I., Baquero F., Martinez J. L. 2006; Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci U S A 103:19484–19489
    [Google Scholar]
  62. Lucchetti-Miganeh C., Burrowes E., Baysse C., Ermel G. 2008; The post-transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 154:16–29
    [Google Scholar]
  63. Lyon G. J., Novick R. P. 2004; Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25:1389–1403
    [Google Scholar]
  64. Marr A. K., Overhage J., Bains M., Hancock R. E. W. 2007; The Lon protease of Pseudomonas aeruginosa is induced by aminoglycosides and is involved in biofilm formation and motility. Microbiology 153:474–482
    [Google Scholar]
  65. Mayville P., Ji G., Beavis R., Yang H., Goger M., Novick R. P., Muir T. W. 1999; Structure–activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc Natl Acad Sci U S A 96:1218–1223
    [Google Scholar]
  66. Michael B., Smith J. N., Swift S., Heffron F., Ahmer B. M. M. 2001; SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 183:5733–5742
    [Google Scholar]
  67. Miller J. C., Stevenson B. 2004; Increased expression of Borrelia burgdorferi factor H-binding surface proteins during transmission from ticks to mice. Int J Med Microbiol 293:120–125
    [Google Scholar]
  68. 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. Mol Cell 15:677–687
    [Google Scholar]
  69. Morris R. O. 1995; Genes specifying auxin and cytokinin biosynthesis in prokaryotes. In Plant Hormones: Physiology, Biochemistry and Molecular Biology, 2nd edn. pp 318–339 Edited by Davies P. J. Dordrecht: Kluwer;
    [Google Scholar]
  70. Nakayama J., Cao Y., Horii T., Sakuda S., Akkermans A. D., de Vos W. M., Nagasawa H. 2001; Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol Microbiol 41:145–154
    [Google Scholar]
  71. Newman K. L., Almeida R. P. P., Purcell A. H., Lindow S. E. 2004; Cell–cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proc Natl Acad Sci U S A 101:1737–1742
    [Google Scholar]
  72. Newman K. L., Chatterjee S., Ho K. A., Lindow S. E. 2008; Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors. Mol Plant Microbe Interact 21:326–334
    [Google Scholar]
  73. Otto M., Echner H., Voelter W., Gotz F. 2001; Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69:1957–1960
    [Google Scholar]
  74. Patten C. L., Glick B. R. 1996; Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220
    [Google Scholar]
  75. Patten C. L., Glick B. R. 2002; Regulation of indoleacetic acid production in Pseudomonas putida GR12-2 by tryptophan and the stationary-phase sigma factor RpoS. Can J Microbiol 48:635–642
    [Google Scholar]
  76. Pearson J. P., Gray K. M., Passador L., Tucker K. D., Eberhard A., Iglewski B. H., Greenberg E. P. 1994; Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci U S A 91:197–201
    [Google Scholar]
  77. Pearson J. P., Passador L., Iglewski B. H., Greenberg E. P. 1995; A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92:1490–1494
    [Google Scholar]
  78. Pearson J. P., Pesci E. C., Iglewski B. H. 1997; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767
    [Google Scholar]
  79. Pei D. H., Zhu J. G. 2004; Mechanism of action of S-ribosylhomocysteinase (LuxS. Curr Opin Chem Biol 8:492–497
    [Google Scholar]
  80. Peng H. L., Novick R. P., Kreiswirth B., Kornblum J., Schlievert P. 1988; Cloning, characterization, and sequencing of an accessory gene regulator ( agr) in Staphylococcus aureus. J Bacteriol 170:4365–4372
    [Google Scholar]
  81. Poplawsky A. R., Chun W. 1998; Xanthomonas campestris pv. campestris requires a functional pigB for epiphytic survival and host infection. Mol Plant Microbe Interact 11:466–475
    [Google Scholar]
  82. Poplawsky A. R., Chun W. 1999; The Xanthomonas campestris pv. campestris DF pheromone and additional regulatory functions of the pig gene cluster. Phytopathology 89:S61
    [Google Scholar]
  83. Poplawsky A. R., Chun W., Slater H., Daniels M. J., Dow J. M. 1998; Synthesis of extracellular polysaccharide, extracellular enzymes, and xanthomonadin in Xanthomonas campestris: evidence for the involvement of two intercellular regulatory signals. Mol Plant Microbe Interact 11:68–70
    [Google Scholar]
  84. Poplawsky A. R., Walters D. M., Rouviere P. E., Chun W. 2005; A gene for a dioxygenase-like protein determines the production of the DF signal in Xanthomonas campestris pv. campestris. Mol Plant Pathol 6:653–657
    [Google Scholar]
  85. Prasad C. 1995; Bioactive cyclic dipeptides. Peptides 16:151–164
    [Google Scholar]
  86. Rather P. N., Orosz E. 1994; Characterization of aarA, a pleiotropic negative regulator of the 2′- N-acetyltransferase in Providencia stuartii. J Bacteriol 176:5140–5144
    [Google Scholar]
  87. Rather P. N., Parojcic M. M., Paradise M. R. 1997; An extracellular factor regulating expression of the chromosomal aminoglycoside 2′- N-acetyltransferase of Providencia stuartii. Antimicrob Agents Chemother 41:1749–1754
    [Google Scholar]
  88. Reading N. C., Sperandio V. 2006; Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254:1–11
    [Google Scholar]
  89. Reading N. C., Torres A. G., Kendall M. M., Hughes D. T., Yamamoto K., Sperandio V. 2007; A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. J Bacteriol 189:2468–2476
    [Google Scholar]
  90. Rezzonico F., Duffy B. 2007; The role of luxS in the fire blight pathogen Erwinia amylovora is limited to metabolism and does not involve quorum sensing. Mol Plant Microbe Interact 20:1284–1297
    [Google Scholar]
  91. Rickard A. H., Palmer R. J., Blehert D. S., Campagna S. R., Semmelhack M. F., Egland P. G., Bassler B. L., Kolenbrander P. E. 2006; Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol 60:1446–1456
    [Google Scholar]
  92. Riedel K., Hentzer M., Geisenberger O., Huber B., Steidle A., Wu H., Høiby N., Givskov M., Molin S., Eberl L. 2001; N-Acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147:3249–3262
    [Google Scholar]
  93. Roche D. M., Byers T. J., Smith D. S., Glansdorp F. G., Spring D. R., Welch M. 2004; Communications blackout? Do N-acylhomoserine-lactone-degrading enzymes have any role in quorum sensing?. Microbiology 150:2023–2028
    [Google Scholar]
  94. Ryan R. P., Fouhy Y., Lucey J. F., Crossman L. C., Spiro S., He Y. W., Zhang L. H., Heeb S., Cámara M. other authors 2006; Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103:6712–6717
    [Google Scholar]
  95. Ryan R. P., Fouhy Y., Fernandez-Garcia B., Watt S. A., Niehaus K., Yang L., Tolker-Nielsen T., Dow J. M. 2008; Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68:75–86
    [Google Scholar]
  96. Schauder S., Bassler B. L. 2001; The languages of bacteria. Genes Dev 15:1468–1480
    [Google Scholar]
  97. Seshasayee A. S. N., Bertone P., Fraser G. M., Luscombe N. M. 2006; Transcriptional regulatory networks in bacteria: from input signals to output responses. Curr Opin Microbiol 9:511–519
    [Google Scholar]
  98. Shikura N., Yamamura J., Nihira T. 2002; barS1, a gene for biosynthesis of a gamma-butyrolactone autoregulator, a microbial signaling molecule eliciting antibiotic production in Streptomyces species. J Bacteriol 184:5151–5157
    [Google Scholar]
  99. Sircili M. P., Walters M., Trabulsi L. R., Sperandio V. 2004; Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect Immun 72:2329–2337
    [Google Scholar]
  100. Slater H., Alvarez-Morales A., Barber C. E., Daniels M. J., Dow J. M. 2000; A two-component system involving an HD-GYP domain protein links cell–cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38:986–1003
    [Google Scholar]
  101. Sperandio V., Mellies J. L., Delahay R. M., Frankel G., Crawford J. A., Nguyen W., Kaper J. B. 2000; Activation of enteropathogenic Escherichia coli (EPEC) LEE2 and LEE3 operons by Ler. Mol Microbiol 38:781–793
    [Google Scholar]
  102. Sperandio V., Li C. Y. C., Kaper J. B. 2002a; Quorum-sensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 70:3085–3093
    [Google Scholar]
  103. Sperandio V., Torres A. G., Kaper J. B. 2002b; 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 43:809–821
    [Google Scholar]
  104. Sperandio V., Torres A. G., Jarvis B., Nataro J. P., Kaper J. B. 2003; Bacteria–host communication: the language of hormones. Proc Natl Acad Sci U S A 100:8951–8956
    [Google Scholar]
  105. Starner T. D., Shrout J. D., Parsek M. R., Appelbaum P. C., Kim G. 2008; Subinhibitory concentrations of azithromycin decrease nontypeable Haemophilus influenzae biofilm formation and diminish established biofilms. Antimicrob Agents Chemother 52:137–145
    [Google Scholar]
  106. Stevenson B., Babb K. 2002; LuxS-mediated quorum sensing in Borrelia burgdorferi, the Lyme disease spirochete. Infect Immun 70:4099–4105
    [Google Scholar]
  107. Stevenson L. G., Strisovsky K., Clemmer K. M., Bhatt S., Freeman M., Rather P. N. 2007; Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase. Proc Natl Acad Sci U S A 104:1003–1008
    [Google Scholar]
  108. Sun J., Daniel R., Wagner-Doebler I., Zeng A.-P. 2004; Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol Biol 4:36
    [Google Scholar]
  109. Surette M. G., Bassler B. L. 1999; Regulation of autoinducer production in Salmonella typhimurium. Mol Microbiol 31:585–595
    [Google Scholar]
  110. 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. Mol Microbiol 42:777–793
    [Google Scholar]
  111. Taga M. E., Miller S. T., Bassler B. L. 2003; Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol Microbiol 50:1411–1427
    [Google Scholar]
  112. Theunis M., Kobayashi H., Broughton W. J., Prinsen E. 2004; Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Mol Plant Microbe Interact 17:1153–1161
    [Google Scholar]
  113. Tomasz A. 1965; Control of component state in Pneumococcus by a hormone-like cell product – an example for a new type of regulatory mechanism in bacteria. Nature 208:155–160
    [Google Scholar]
  114. Tortosa P., Logsdon L., Kraigher B., Itoh Y., Mandic-Mulec I., Dubnau D. 2001; Specificity and genetic polymorphism of the Bacillus competence quorum-sensing system. J Bacteriol 183:451–460
    [Google Scholar]
  115. Tsui W. H. W., Yim G., Wang H. H. M., McClure J. E., Surette M. G., Davies J. 2004; Dual effects of MLS antibiotics: transcriptional modulation and interactions on the ribosome. Chem Biol 11:1307–1316
    [Google Scholar]
  116. Upton M., Tagg J. R., Wescombe P., Jenkinson H. F. 2001; Intra- and interspecies signaling between Streptococcus salivarius and Streptococcus pyogenes mediated by SalA and SalA1 lantibiotic peptides. J Bacteriol 183:3931–3938
    [Google Scholar]
  117. Verstrepen K. J., Reynolds T. B., Fink G. R. 2004; Origins of variation in the fungal cell surface. Nat Rev Microbiol 2:533–540
    [Google Scholar]
  118. Walters M., Sircili M. P., Sperandio V. 2006; AI-3 synthesis is not dependent on luxS in Escherichia coli. J Bacteriol 188:5668–5681
    [Google Scholar]
  119. Wang D. D., Ding X. D., Rather P. N. 2001; Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183:4210–4216
    [Google Scholar]
  120. Wang L. H., He Y., Gao Y., Wu J. E., Dong Y. H., He C., Wang S. X., Weng L. X., Xu J. L. other authors 2004; A bacterial cell–cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903–912
    [Google Scholar]
  121. Waters C. M., Bassler B. L. 2005; Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346
    [Google Scholar]
  122. Whatmore A. M., Barcus V. A., Dowson C. G. 1999; Genetic diversity of the streptococcal competence ( com) gene locus. J Bacteriol 181:3144–3154
    [Google Scholar]
  123. Whitehead N. A., Barnard A. M. L., Slater H., Simpson N. J. L., Salmond G. P. C. 2001; Quorum-sensing in gram-negative bacteria. FEMS Microbiol Rev 25:365–404
    [Google Scholar]
  124. Winzer K., Hardie K. R., Williams P. 2002; Bacterial cell-to-cell communication: sorry, can't talk now – gone to lunch!. Curr Opin Microbiol 5:216–222
    [Google Scholar]
  125. Xavier K. B., Bassler B. L. 2003; LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6:191–197
    [Google Scholar]
  126. Xavier K. B., Bassler B. L. 2005; Interference with AI-2-mediated bacterial cell-cell communication. Nature 437:750–753
    [Google Scholar]
  127. Xavier K. B., Miller S. T., Lu W. Y., Kim J. H., Rabinowitz J., Pelczer I., Semmelhack M. F., Bassler B. L. 2007; Phosphorylation and processing of the quorum-sensing molecule autoinducer-2 in enteric bacteria. ACS Chem Biol 2:128–136
    [Google Scholar]
  128. Yao Y., Martinez-Yamout M. A., Dickerson T. J., Brogan A. P., Wright P. E., Dyson H. J. 2006; Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J Mol Biol 355:262–273
    [Google Scholar]
  129. Yim G., Wang H. H. M., Davies J. 2006; The truth about antibiotics. Int J Med Microbiol 296:163–170
    [Google Scholar]
  130. Yim G., Wang H. M. H., Davies J. 2007; Antibiotics as signalling molecules. Philos Trans R Soc London B Biol Sci 362:1195–1200
    [Google Scholar]
  131. Zhang L. L., Jia Y. T., Wang L., Fang R. X. 2007; A proline iminopeptidase gene upregulated in planta by a LuxR homologue is essential for pathogenicity of Xanthomonas campestris pv. campestris. Mol Microbiol 65:121–136
    [Google Scholar]
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