Advertisement

Antonie van Leeuwenhoek

, Volume 74, Issue 4, pp 199–210 | Cite as

Quorum sensing and the cell-cell communication dependent regulation of gene expression in pathogenic and non-pathogenic bacteria

  • Andrea M. Hardman
  • Gordon S.A.B. Stewart
  • Paul WilliamsEmail author
Article

Abstract

Although it has been clear for some time that individual bacterial cells employ intra-cellular signalling systems to sense, integrate and process information from their surroundings, their widespread capacity to perceive information from other bacterial cells is only just beginning to be recognised. Recent work has established that diverse bacteria exploit a cell-cell communication device to regulate the transcription of multiple target genes. This communication device termed ‘quorum sensing’, depends on the production of one or more diffusible signal molecules termed ‘autoinducers’ or ‘pheromones’ which enable a bacterium to monitor its own cell population density. Quorum sensing is thus an example of multicellular behaviour in prokaryotes and regulates diverse physiological processes including bioluminescence, swarming, antibiotic biosynthesis, plasmid conjugal transfer and the production of virulence determinants in animal, fish and plant pathogens. In Gram-negative bacteria, the best understood family of signal molecules are the N-acylhomoserine lactones (AHLs) which vary predominantly in the presence or absence of an acyl chain C3 substituent (oxo- or hydroxy-) and length of the N-acyl side chain. However not all quorum sensing signal molecules are AHLs; in Gram-positive bacteria, they are often post-translationally modified peptides. Irrespective of the chemical ‘language’ employed, interference with either the synthesis or transmission of a quorum sensing signal molecule in pathogenic bacteria offers an exciting new strategy for controlling infection.

Quorum sensing N-acylhomoserine lactones gene expression virulence secondary metabolites 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bainton NJ, Bycroft BW, Chhabra SR, Stead P, Gledhill L, Hill PJ, Rees CED, Winson MK, Salmond GPC, Stewart GSAB & Williams P (1992a) A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene 116: 87–91Google Scholar
  2. Bainton NJ, Stead P, Chhabra SR, Bycroft BW, Salmond GPC, Stewart, GSAB & Williams P (1992b) N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288: 997–1004Google Scholar
  3. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJG, Slater H, Dow JM, Williams P & Daniels MJ (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol. Microbiol. 24: 555–566Google Scholar
  4. Beck von Bodman S & Farrand SK (1995) Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J. Bacteriol. 177: 5000–5008Google Scholar
  5. Brint JM & Ohman DE (1995) Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J. Bacteriol. 177: 7155–7163Google Scholar
  6. Bycroft BW, Maslen C, Box SJ, Brown AG & Tyler JW (1987) The isolation and characterisation of (3R,5R)-carbapenam-3-carboxylic and (3S,5R)-carbapenam-3-carboxylic acid from Serratia and Erwinia species and their putative biosynthetic role. J. Chem. Soc. Chem. Comm. 1623–1625Google Scholar
  7. Cao JG & Meighen EA (1989) Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J. Biol. Chem. 264: 21670–21676Google Scholar
  8. Chapon-Herv & #x00E9; V, Akrim M, Latifi A, Williams P, Lazdunski A & Bally M (1997) Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol. Microbiol. 24: 1169–1178Google Scholar
  9. Clewell DB (1990) Movable genetic elements and antibiotic-resistance in enterococci. Eur. J. Clin. Microbiol. Infect. Dis. 9: 90–102Google Scholar
  10. Cubo MT, Economou A, Murphy G, Johnston AWB & Downie JA (1992) Molecular characterisation and regulation of the rhizosphere-expressed genes rhiABC that can influence nodulation by Rhizobium leguminosarum biovar viciae. J. Bacteriol. 174: 4026–4035Google Scholar
  11. Dorman C & Bhriain N (1992) Global regulation of gene expression during environmental adaptation: implications for bacterial pathogens. In: Hormaeche CE, Penn CW & Smith CJ (Eds) Molecular Biology of Bacterial Infections (pp 193–230). Cambridge University PressGoogle Scholar
  12. Dunphy G, Miyamoto C & Meighen E (1997) A homoserine lactone autoinducer regulates virulence of an insect-pathogenic bacterium Xenorhabdus nematophilus (Enterobacteriaceae). J. Bacteriol. 179: 5288–5291Google Scholar
  13. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH & Oppenheimer NJ (1981) Structural identification of the autoinducer of Photobacterium fischeri luciferase. Biochemistry 20: 2444–2449Google Scholar
  14. Eberhard A, Widrig CA, McBath P & Schineller JB (1986) Analogs of the autoinducer of bioluminesence in Vibrio fischeri. Arch. Microbiol. 146: 35–40Google Scholar
  15. Eberl L, Winson MK, Stenberg C, Stewart GSAB, Christiansen G, Chhabra SR, Bycroft BW, Williams P, Molin S & Givskov M (1996) Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20: 127–136Google Scholar
  16. Engebrecht J & Silverman M (1984) Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. USA 81: 4154–4158Google Scholar
  17. — (1987) Nucleotide sequence of the regulatory locus controlling expression of bacterial genes for bioluminescence. Nucleic Acids Res. 15: 10455–10467Google Scholar
  18. Flavier AB, Clough SJ, Schell MA & Denny TP (1997a) Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol. Microbiol. 26: 251–259Google Scholar
  19. Flavier AB, Ganova-Raeva LM, Schell MA & Denny TP (1997b) Hierarchical autoinduction in Ralstonia solanacearum: control of acyl-homoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester. J. Bacteriol. 179: 7089–7097Google Scholar
  20. Fuqua WC & Winans (1994) A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumour metabolite. J. Bacteriol. 176: 2796–2806Google Scholar
  21. Fuqua WC, Winans SC & Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269–275Google Scholar
  22. — (1996) Census and consensus in bacterial ecosystems: The LuxR-LuxI family of quorum sensing transcriptional regulators. Ann. Rev. Microbiol. 727–751Google Scholar
  23. Gamard P, Sauriol F, Benhamou N, Belanger RR & Paulitz TC (1997) Novel butyrolactones with antifungal activity produced by Pseudomonas aureofaciens strain 63–28. J. Antibiotics 50: 742–749Google Scholar
  24. Gambello MJ & Iglewski BH (1991) Cloning and characterisation of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J. Bacteriol. 173: 3000–3009Google Scholar
  25. Gilson L, Kuo A & Dunlap PV (1995) AinS and a new family of autoinducer synthesis proteins J. Bacteriol. 177: 6946–6951Google Scholar
  26. Givskov M, de Nys R, Manefield M, Gram L, Maximilien R, Eberl L, Soren M, Steinberg PD & Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178: 6618–6622Google Scholar
  27. Govan JRW & Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60: 539Google Scholar
  28. Gray KM, Passador L, Iglewski BH & Greenberg EP (1994) Interchangeability and specificity of components from the quorum sensing regulatory systems of Vibrio fischeri and Pseudomonas aeruginosa. J. Bacteriol. 176: 3076–3080Google Scholar
  29. Gray KM, Pearson JP, Downie JA, Boboye BB & Greenberg EP (1996) Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178: 372–376Google Scholar
  30. Grossman AD (1995) Genetic networks controlling the initiation of sporulation and the development of competence in Bacillus subtilis. Ann. Rev. Genetics 29: 477–508Google Scholar
  31. Harshey RM (1994) Bees aren & #x2019;t the only ones-swarming in Gramnegative bacteria. Mol. Microbiol. 13: 389–394Google Scholar
  32. Håvarstein LS, Coomaraswamy G & Morrison DA (1995) An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 92: 11140–11144Google Scholar
  33. Hengge-Aronis R (1993) Survival of hunger and stress: the role of RpoS in early stationary phase gene regulation in Escherichia coli. Cell 72: 165–168Google Scholar
  34. Horinouchi S & Beppu T (1992) Autoregulatory factors and communication in actinomycetes Ann. Rev. Micobiol. 46: 377–398Google Scholar
  35. Hwang IY, Li PL, Zhang LH, Piper KR, Cook DM, Tate ME & Farrand SK (1994) TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. Proc. Natl. Acad. Sci. USA 91: 4639–4643Google Scholar
  36. Ji G, Beavis RC & Novick RP (1995) Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc. Natl.Acad. Sci USA 92: 12055–12059Google Scholar
  37. — (1997) Bacterial interference caused by autoinducing peptide variants. Science 276: 2027–2030Google Scholar
  38. Jiang Y, Camara M, Chhabra SR, Hardie KR, Bycroft BW, Lazdunski A, Salmond GPC, Stewart GSAB & Williams P (1998). In vitro biosynthesis of the Pseudomonas aeruginosa quorum sensing signal molecule, N-butanoyl-L-homoserine lactone. Mol. Microbiol. 28: 193–205Google Scholar
  39. Jones S, Yu B, Bainton NJ, Birdsall M, Bycroft BW, Chhabra SR, Cox AJR, Golby P, Reeves PJ, Stephens S, Winson MK, Salmond GPC, Stewart G & Williams P (1993) The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 12: 2477–2482Google Scholar
  40. Kaplan HB & Greenberg EP (1985) Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J. Bacteriol. 163: 1210–1214Google Scholar
  41. Kleerebezem M, Quadri LEN, Kuipers OP & de Vos WM (1997) Quorum sensing by peptide pheromones and two component signal transduction systems in Gram-positive bacteria. Mol. Microbiol. 24: 895–904Google Scholar
  42. Kuo A, Blough NV & Dunlap PV. (1994) Multiple N-acyl-L-homoserine lactone autoinducers of luminescence in the marine symbiotic bacterium Vibrio fischeri. J. Bacteriol. 178: 971–976Google Scholar
  43. Kuspa A, Plamann L & Kaiser D (1992) A-signalling and the cell density requirement for Myxococcus xanthus development. J. Bacteriol. 174: 7360–7369Google Scholar
  44. Latifi A, Winson MK, Foglino M, Bycroft BW, Stewart GSAB, Lazdunski A & Williams P (1995) Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 17: 333–343Google Scholar
  45. Latifi A, Foglino M, Tanaka K, Williams P & Lazdunski A (1996) A hierarchical quorum sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21: 1137–1146Google Scholar
  46. Magnuson R, Solomon J & Grossman AD (1994) Biochemical and genetic characterization of a competence pheromone from Bacillus subtilis. Cell 77: 207–216Google Scholar
  47. McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GSAB & Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143: 3703–3711Google Scholar
  48. McGowan S, Sebaihia M, Jones S, Yu B, Bainton N, Chan PF, Bycroft B, Stewart GSAB, Williams P & Salmond GPC (1995) Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator. Microbiology 141: 541–550Google Scholar
  49. McGowan SJ, Sebaihia M, Porter LE, Stewart GSAB, Williams P, Bycroft, BW & Salmond GPC (1996) Analysis of bacterial carbapenem antibiotic production genes reveals a novel ß-lactam biosynthesis pathway. Mol. Microbiol. 22: 415–426Google Scholar
  50. McGowan SJ, Sebaihia, M, O & #x2019;Leary, S, Hardie, KR, Williams P, Stewart GSAB, Bycroft BW & Salmond GPC (1997) Analysis of the carbapenem gene cluster of Erwinia carotovora: definition of the antibiotic biosynthetic genes and evidence for a novel ßlactam resistance mechanism. Mol. Microbiol 26: 545–556Google Scholar
  51. Milton DL, Hardman A, Camara M, Chhabra SR, Bycroft BW, Stewart GSAB & Williams P (1997) Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone. J. Bacteriol. 179: 3004–3012Google Scholar
  52. Mor & #x00E9; MI, Finger LD, Stryker JL, Fuqua C, Eberhard A & Winans SC (1996) Enzymatic synthesis of a quorum sensing autinducer through use of defined substrates. Science 272: 1655–1658Google Scholar
  53. Nealson KH (1977) Autoinduction of bacterial luciferase: occurrence, mechanism and significance. Microbiol. Rev. 43: 496–518Google Scholar
  54. Nealson KH, Platt T & Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system J. Bacteriol. 104: 313–322Google Scholar
  55. Ochsner UA & Reiser J (1995) Autoinducer mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92: 6424–6428Google Scholar
  56. Ochsner UA, Koch A, Fiechter A & Reiser J (1994) Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J. Bacteriol. 176: 2044–2054Google Scholar
  57. Parker WL, Rathnum ML, Wells JS, Trejo WH, Principe PA & Sykes RB (1982) SQ 27,860, a simple carbapenem produced by species of Serratia and Erwinia. J. Antibiotics 35: 653–660Google Scholar
  58. Parkinson JS & Kofoid EC (1992) Communication modules in bacterial signalling proteins. Ann. Rev. Genetics 26: 71–112Google Scholar
  59. Passador L, Cook JM, Gambello MJ, Rust L & Iglewski BH (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260: 1127–1130Google Scholar
  60. Pearson JP, Gray KM, Passador L, Tucker KD, Eberhard A, Iglewski BH & Greenberg EP (1994) Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91: 197–201Google Scholar
  61. Pearson JP, Passador L, Iglewski BH & Greenberg EP (1995) A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92: 1490–1494Google Scholar
  62. Pearson JP, Pesci EC & Iglewski BH. (1997) Roles of Pseudomonas aeruginosa las and rhl quorum sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol. 179: 5756–5767Google Scholar
  63. Pesci EC, Pearson JP, Seed PC & Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179: 3127–3132Google Scholar
  64. Pestova EV, Håvarstein LS, Morrison DA (1996) Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a twocomponent regulatory system. Mol. Microbiol. 21: 853–862Google Scholar
  65. Pierson LS, Kepenne VD & Wood DW (1994) Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30–84 is regulated by PhzR in response to cell density. J. Bacteriol. 176: 3966–3974Google Scholar
  66. Piper KR, Beck von Bodman S & Farrand SK (1993) Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362: 448–450Google Scholar
  67. Pirhonen M, Saarilahti H, Karlsson MB & Palva ET (1991) Identification of pathogenicity determinants of Erwinia carotovora subsp. carotovora by transposon mutagenesis. Mol. Plant-Microbe Interact. 4: 276–283Google Scholar
  68. Pollack M (1990) Pseudomonas aeruginosa. In: Mandell GL, Douglas RG & Bennett JE (Eds) Principles and Practice of Infectious Disease (pp 1673–1691). Churchill Livingstone Press Inc., New YorkGoogle Scholar
  69. Puskas A, Greenberg EP, Kaplan S & Schaefer AL (1997) A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides. J. Bacteriol. 179: 7530–7537Google Scholar
  70. Salmond GPC, Bycroft BW, Stewart GSAB & Williams P (1995) The bacterial enigma: cracking the code of cell–cell communication. Mol. Microbiol. 16: 615–624Google Scholar
  71. Salzmann TN, Ratcliffe, RW, Christensen BG & Bouffard FA (1980) A sterocontrolled, enantiomerically specific total synthesis of thienomycin. Phil. Trans. R. Soc. Lond. 289: 191–195Google Scholar
  72. Schaefer AL, Hanzelka BL, Eberhard A & Greenberg EP (1996a) Quorum sensing in Vibrio fischeri: probing autoinducer LuxR interactions with autoinducer analogs. J. Bacteriol. 178: 2897–2901Google Scholar
  73. Schaefer AL, Val DL, Hanzelka BL, Cronan JE & Greenberg EP (1996b) Generation of cell-to-cell signals in quorum sensing: acylhomoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. USA 93: 9505–9509Google Scholar
  74. Schripsema J, de Rudder KEE, van Vliet TB, Lankhorst PP, de Vroom E, Kijne JW & van Brussel AA (1996) Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-L-homoserine lactone molecules known as autoinducers and as quorum sensing co-transcriptional factors. J. Bacteriol. 178: 366–371Google Scholar
  75. Shapiro JA (1988) Bacteria as multicellular organisms. Scientific Amer. 256: 82–89Google Scholar
  76. Shaw PD, Ping G, Daly S, Cronan JE, Rhinehart K & Farrand SK (1997) Detecting and characterizing acyl-homoserine lactone signal molecules by thin layer chromatography. Proc. Natl. Acad. Sci. USA 94: 6036–6041Google Scholar
  77. Stephens K (1986) Pheromones among the prokaryotes. CRC Critical Rev. Microbiol. 113: 309–334Google Scholar
  78. Stevens AM, Dolan KM & Greenberg EP (1994) Synergistic binding of the Vibrio fischeri LuxR transcriptional activator domain and RNA polymerase to the lux promoter region. Proc. Natl. Acad. Sci. USA 91: 12619–12623Google Scholar
  79. Swift S, Winson MK, Chan PF, Bainton NJ, Birdsall M, Reeves PJ, Rees CED, Chhabra SR, Hill PJ, Throup JP, Bycroft BW, Salmond GPC, Williams P & Stewart G (1993) A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria. Mol. Microbiol. 10: 511–520Google Scholar
  80. Swift S, Throup JP, Williams P, Salmond GPC & Stewart, GSAB (1996) Quorum sensing: a population density component in the determinantion of bacterial phenotype. TIBS 21: 214–219Google Scholar
  81. Swift S, Karlyshev AV, Fish L, Durant E, Winson MK, Chhabra SR, Williams P, MacIntyre S & Stewart GSAB (1997) Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J. Bacteriol. 179: 5271–5281Google Scholar
  82. Tang HB, Dimango E, Bryan R, Gambello MJ, Iglewski BH, Goldberg JB & Prince A (1996) Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect. Immun. 64: 37–43Google Scholar
  83. Telford G, Wheeler D, Williams P, Tomkins PT, Appleby P, Sewell H, Stewart GSAB, Bycroft, BW & Pritchard DI (1998) The Pseudomonas aeruginosa quorum sensing signal molecule, N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity. Infect. Immun. 66: 36–42Google Scholar
  84. Throup JP, Camara M, Briggs GS, Winson MK, Chhabra SR, Bycroft BW, Williams P & Stewart GSAB (1995a) Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules. Mol. Microbiol. 17: 345–356Google Scholar
  85. Throup J, Winson MK, Bainton NJ, Bycroft BW, Williams P & Stewart GSAB (1995b). Signalling in bacteria beyond bioluminescence. In: Campbell A, Kricka L & Stanley P (Eds) Bioluminescence and Chemiluminescence: Fundamentals and Applied Aspects (pp 89–92) John Wiley & Sons, Chichester, U.K.Google Scholar
  86. Waldburger C, Gonzalez D & Chambliss GH (1993) Characterization of a new sporulation factor in Bacillus subtilis. J. Bacteriol. 175: 6321–6327Google Scholar
  87. Williams P (1994) Compromising bacterial communication skills. J. Pharm. Pharmacol. 46: 252–260Google Scholar
  88. Williams P, Bainton NJ, Swift S, Chhabra SR, Winson MK, Stewart GSAB, Salmond GPC & Bycroft BW (1992) Small molecule-mediated density-dependent control of gene expression in prokaryotes: bioluminescence and the biosynthesis of carbapenem antibiotics. FEMS Microbiol. Lett. 100: 161–167Google Scholar
  89. Williams P, Stewart GSAB, Camara M, Winson MK, Chhabra SR, Salmond GPC & Bycroft BW (1996) Signal transduction through quorum sensing in Pseudomonas aeruginosa. In: Nakazawa T, Furukawa K, Kaas D & Silver S (Eds) Molecular Biology of the Pseudomonads (pp 195–205) ASM Press, Washington DCGoogle Scholar
  90. Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR, Daykin M, Bally M, Chapon V, Salmond GPC, Bycroft BW, Lazdunski A, Stewart GSAB & Williams P (1995) Multiple N-acylhomoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92: 9427–9431Google Scholar
  91. Wirth R, Muscholl A & Wanner G (1996) The role of pheromones in bacterial interactions. Trends Microbiol. 4: 96–103Google Scholar
  92. Wood DW, Gong F, Daykin M, Williams P & Pierson LS (1997) Nacylhomoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30–84 in the wheat rhizosphere. J. Bacteriol. 179: 7663–7670Google Scholar
  93. Zhang LH, Murphy PJ, Kerr A & Tate ME (1993) Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature 362: 446–448Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Andrea M. Hardman
    • 1
  • Gordon S.A.B. Stewart
    • 1
  • Paul Williams
    • 1
    • 2
    Email author
  1. 1.Department of Pharmaceutical SciencesUniversity of NottinghamNottinghamU.K
  2. 2.Institute of Infections and Immunity, Queens Medical CentreUniversity of NottinghamNottinghamU.K

Personalised recommendations