Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone
10.1128/jb.179.9.3004-3012.1997
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

Certain gram-negative pathogens are known to control virulence gene expression through cell-cell communication via small diffusible signal molecules termed autoinducers. This intercellular signal transduction mechanism termed quorum sensing depends on the interaction of an N-acylhomoserine lactone (AHL) auto-inducer molecule with a receptor protein belonging to the LuxR family of positive transcriptional activators. Vibrio anguillarum is a gram-negative pathogen capable of causing a terminal hemorrhagic septicemia known as vibriosis in fish such as rainbow trout. In this study, we sought to determine whether V. anguillarum employs AHLs to regulate virulence gene expression. Spent V. anguillarum culture supernatants stimulated bioluminescence in a recombinant lux-based Escherichia coli AHL biosensor strain, whereas they both stimulated and inhibited AHL-mediated violacein pigment production in Chromobacterium violaceum. This finding suggested that V. anguillarum may produce multiple AHL signal molecules. Using high-performance liquid chromatography and high-resolution tandem mass spectrometry, we identified the major V. anguillarum AHL as N-(3-oxodecanoyl)-L-homoserine lactone (ODHL), a structure which was unequivocally confirmed by chemical synthesis. The gene (vanI) responsible for ODHL synthesis was cloned and sequenced and shown to belong to the LuxI family of putative AHL synthases. Further sequencing downstream of vanI revealed a second gene (vanR) related to the LuxR family of transcriptional activators. Although deletion of vanI abolished ODHL synthesis, no reduction of either metalloprotease production or virulence in a fish infection model was observed. However, the vanI mutant remained capable of weakly activating both bioluminescence and violacein in the E. coli and C. violaceum biosensors, respectively, indicating the existence of additional layers of AHL-mediated regulatory complexity.

Bibliography

Milton, D. L., Hardman, A., Camara, M., Chhabra, S. R., Bycroft, B. W., Stewart, G. S., & 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. Journal of Bacteriology, 179(9), 3004–3012.

Authors 7
  1. D L Milton (first)
  2. A Hardman (additional)
  3. M Camara (additional)
  4. S R Chhabra (additional)
  5. B W Bycroft (additional)
  6. G S Stewart (additional)
  7. P Williams (additional)
References 59 Referenced 138
  1. Bainton , N. J. , B. W. Bycroft , S. R. Chhabra , P. Stead , L. Gledhill , L. P. J. Hill , C. E. D. Rees , M. K. Winson , G. P. C. Salmond , G. S. A. B. Stewart , and P. Williams . 1992 . A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia . Gene 116 : 87 - 91 . (10.1016/0378-1119(92)90633-Z) / Gene / A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia by Bainton N. J. (1992)
  2. Bainton N. J. P. Stead S. R. Chhabra B. W. Bycroft G. P. C. Salmond G. S. A. B. Stewart and P. Williams. 1992. N-(3-Oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora Biochem. J. 288:997-1004. (10.1042/bj2880997)
  3. Bassler , B. L. , M. Wright , R. E. Showalter , and M. R. Silverman . 1993 . Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of Iuminescence. Mol. Microbiol. 9 : 773 - 786 . (10.1111/j.1365-2958.1993.tb01737.x) / Iuminescence. Mol. Microbiol. / Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of by Bassler B. L. (1993)
  4. Beck von Bodman , S. , and S. K. Farrand . 1995 . Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer . J. Bacteriol. 177 : 5000 - 5008 . (10.1128/JB.177.17.5000-5008.1995) / J. Bacteriol. / Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer by Beck von Bodman S. (1995)
  5. Cao , J. - G. , and E. A. Meighen . 1989 . Purification and structural identification of an autoinducer for the Iuminescence system of V. harveyi . J. Biol. Chem. 264 : 21670 - 21676 . (10.1016/S0021-9258(20)88238-6) / J. Biol. Chem. / Purification and structural identification of an autoinducer for the Iuminescence system of V. harveyi by Cao J. (1989)
  6. Cao , J. - G. , and E. A. Meighen . 1993 . Biosynthesis and stereochemistry of the autoinducer controlling Iuminescence in Vibrio harveyi . J. Bacteriol. 175 : 3856 - 3862 . (10.1128/JB.175.12.3856-3862.1993) / J. Bacteriol. / Biosynthesis and stereochemistry of the autoinducer controlling Iuminescence in Vibrio harveyi by Cao J. (1993)
  7. Chhabra , S. R. , P. Stead , N. J. Bainton , G. P. C. Salmond , G. S. A. B. Stewart , P. Williams , and B. W. Bycroft . 1993 . Autoregulation of carbapenem biosynthesis in Erwinia carotovora ATCC 39048 by analogues of N-(3- oxohexanoyl)-L-homoserine lactone . J. Antibiot. 46 : 441 - 454 . (10.7164/antibiotics.46.441) / J. Antibiot. / Autoregulation of carbapenem biosynthesis in Erwinia carotovora ATCC 39048 by analogues of N-(3- oxohexanoyl)-L-homoserine lactone by Chhabra S. R. (1993)
  8. Crosa , J. H. 1989 . Genetics and molecular biology of siderophore-mediated iron transport in bacteria . Microbiol. Rev. 53 : 517 - 530 . (10.1128/mr.53.4.517-530.1989) / Microbiol. Rev. / Genetics and molecular biology of siderophore-mediated iron transport in bacteria by Crosa J. H. (1989)
  9. Devereux , J. , P. Haeberli , and O. Smithies . 1984 . A comprehensive set of sequence analysis programs for the VAX . Nucleic Acids Res. 12 : 387 - 395 . (10.1093/nar/12.1Part1.387) / Nucleic Acids Res. / A comprehensive set of sequence analysis programs for the VAX by Devereux J. (1984)
  10. Devine , J. H. , G. S. Shadel , and T. O. Baldwin . 1989 . Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744 . Proc. Natl. Acad. Sci. USA 86 : 5688 - 5692 . (10.1073/pnas.86.15.5688) / Proc. Natl. Acad. Sci. USA / Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744 by Devine J. H. (1989)
  11. Eberhard , A. , A. L. Burlingame , C. Eberhard , G. L. Kenyon , K. H. Nealson , and N. J. Oppenheimer . 1981 . Structural identification of autoinducer of Photobacterium fischeri Iuciferase . Biochemistry 20 : 2444 - 2449 . (10.1021/bi00512a013) / Biochemistry / Structural identification of autoinducer of Photobacterium fischeri Iuciferase by Eberhard A. (1981)
  12. Eberhard , A. , T. Longin , C. A. Widrig , and S. J. Stranick . 1991 . Synthesis of the lux gene autoinducer in V. fischeri is positively autoregulated . Arch. Microbiol. 155 : 294 - 297 . (10.1007/BF00252215) / Arch. Microbiol. / Synthesis of the lux gene autoinducer in V. fischeri is positively autoregulated by Eberhard A. (1991)
  13. Eberl , L. , M. K. Winson , C. Sternberg , G. S. A. B. Stewart , G. Christiansen , S. R. Chhabra , B. W. Bycroft , P. Williams , S. Molin , and M. Giskov . 1996 . Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens . Mol. Microbiol. 20 : 127 - 136 . (10.1111/j.1365-2958.1996.tb02495.x) / Mol. Microbiol. / Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens by Eberl L. (1996)
  14. Fuqua , W. C. , and S. C. Winans . 1994 . A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite . J. Bacteriol. 176 : 2796 - 2806 . (10.1128/JB.176.10.2796-2806.1994) / J. Bacteriol. / A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite by Fuqua W. C. (1994)
  15. Fuqua , W. C. , S. C. Winans , and E. P. Greenberg . 1994 . Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators . J. Bacteriol. 176 : 269 - 275 . (10.1128/JB.176.2.269-275.1994) / J. Bacteriol. / Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators by Fuqua W. C. (1994)
  16. Gambello , M. J. , and B. H. Iglewski . 1991 . Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression . J. Bacteriol. 173 : 3000 - 3009 . (10.1128/JB.173.9.3000-3009.1991) / J. Bacteriol. / Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression by Gambello M. J. (1991)
  17. Gilson , L. , A. Kuo , and P. V. Dunlap . 1996 . AinS and a new family of autoinducer synthesis proteins . J. Bacteriol. 177 : 6946 - 6951 . (10.1128/JB.177.23.6946-6951.1995) / J. Bacteriol. / AinS and a new family of autoinducer synthesis proteins by Gilson L. (1996)
  18. Gray , K. M. , L. Passador , B. H. Iglewski , and E. P. Greenberg . 1994 . Interchangeability and specificity of components from the quorum-sensing regulatory systems of Vibrio fischeri and Pseudomonas aeruginosa . J. Bacteriol. 176 : 3076 - 3080 . (10.1128/JB.176.10.3076-3080.1994) / J. Bacteriol. / Interchangeability and specificity of components from the quorum-sensing regulatory systems of Vibrio fischeri and Pseudomonas aeruginosa by Gray K. M. (1994)
  19. Gray , K. M. , J. P. Pearson , J. Allan Downie , B. B. Boboye , and E. P. Greenberg . 1996 . Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes . J. Bacteriol. 178 : 372 - 376 . (10.1128/jb.178.2.372-376.1996) / J. Bacteriol. / Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes by Gray K. M. (1996)
  20. Hanzelka , B. L. , and E. P. Greenberg . 1996 . Quorum sensing in Vibrio fischeri: evidence that S-adenosylmethionine is the amino acid substrate for autoinducer synthesis . J. Bacteriol. 178 : 5291 - 5294 . (10.1128/jb.178.17.5291-5294.1996) / J. Bacteriol. / Quorum sensing in Vibrio fischeri: evidence that S-adenosylmethionine is the amino acid substrate for autoinducer synthesis by Hanzelka B. L. (1996)
  21. Hwang , I. , P. -L. Li , L. Zhang , K. R. Piper , D. M. Cook , M. E. Tate , and S. K. Farrand . 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 - 4643 . (10.1073/pnas.91.11.4639) / Proc. Natl. Acad. Sci. USA / TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer by Hwang I. (1994)
  22. Ji , G. Y. , R. C. Beavis , and R. P. Novick . 1995 . Cell density control of staphylococcal virulence mediated by an octapeptide pheromone . Proc. Natl. Acad. Sci. USA 92 : 12055 - 12059 . (10.1073/pnas.92.26.12055) / Proc. Natl. Acad. Sci. USA / Cell density control of staphylococcal virulence mediated by an octapeptide pheromone by Ji G. Y. (1995)
  23. Jones , S. , B. Yu , N. J. Bainton , M. Birdsall , B. W. Bycroft , S. R. Chhabra , A. J. R. Cox , P. Golby , P. J. Reeves , S. Stephens , M. K. Winson , G. P. C. Salmond , G. S. A. B. Stewart , and P. Williams . 1993 . The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa . EMBO J. 12 : 2477 - 2482 . (10.1002/j.1460-2075.1993.tb05902.x) / EMBO J. / The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa by Jones S. (1993)
  24. Kaplan , H. B. , and E. P. Greenberg . 1985 . Diffusion of autoinducer is involved in regulation of the Vibrio fischeri Iuminescence system . J. Bacteriol. 163 : 1210 - 1214 . (10.1128/JB.163.3.1210-1214.1985) / J. Bacteriol. / Diffusion of autoinducer is involved in regulation of the Vibrio fischeri Iuminescence system by Kaplan H. B. (1985)
  25. Kuo , A. , S. M. Callahan , and P. V. Dunlap . 1996 . Modulation of Iuminescence operon expression by N-octanoyl-L-homoserine lactone in ainS mutants of Vibrio fischeri . J. Bacteriol. 178 : 971 - 976 . (10.1128/jb.178.4.971-976.1996) / J. Bacteriol. / Modulation of Iuminescence operon expression by N-octanoyl-L-homoserine lactone in ainS mutants of Vibrio fischeri by Kuo A. (1996)
  26. Latifi , A. , M. K. Winson , M. Foglino , B. W. Bycroft , G. S. A. B. Stewart , A. Lazdunski , and P. Williams . 1995 . Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PA01 . Mol. Microbiol. 17 : 333 - 343 . (10.1111/j.1365-2958.1995.mmi_17020333.x) / Mol. Microbiol. / Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PA01 by Latifi A. (1995)
  27. McGee , K. , P. Hörstedt , and D. Milton . 1996 . Identification and characterization of additional flagellin genes from Vibrio anguillarum . J. Bacteriol. 178 : 5188 - 5198 . (10.1128/jb.178.17.5188-5198.1996) / J. Bacteriol. / Identification and characterization of additional flagellin genes from Vibrio anguillarum by McGee K. (1996)
  28. McGowan , S. , M. Sebaihia , S. Jones , B. Yu , N. Bainton , P. F. Chan , B. Bycroft , G. S. A. B. Stewart , P. Williams , and G. P. C. Salmond . 1995 . Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator . Microbiology 141 : 541 - 550 . (10.1099/13500872-141-3-541) / Microbiology / Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator by McGowan S. (1995)
  29. Meighen , E. A. 1991 . Molecular biology of bacterial bioluminescence . Microbiol. Rev. 55 : 123 - 142 . (10.1128/MR.55.1.123-142.1991) / Microbiol. Rev. / Molecular biology of bacterial bioluminescence by Meighen E. A. (1991)
  30. Meighen , E. A. 1994 . Genetics of bacterial bioluminescence. Annu . Rev. Genet. 28 : 117 - 139 . (10.1146/annurev.ge.28.120194.001001) / Rev. Genet. / Genetics of bacterial bioluminescence. Annu by Meighen E. A. (1994)
  31. Miller , V. L. , and J. J. Mekalanos . 1988 . A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR . J. Bacteriol. 170 : 2575 - 2583 . (10.1128/jb.170.6.2575-2583.1988) / J. Bacteriol. / A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR by Miller V. L. (1988)
  32. Milton , D. L. , A. Norqvist , and H. Wolf-Watz . 1992 . Cloning of a metalloprotease gene involved in the virulence mechanism of Vibrio anguillarum . J. Bacteriol. 174 : 7235 - 7244 . (10.1128/jb.174.22.7235-7244.1992) / J. Bacteriol. / Cloning of a metalloprotease gene involved in the virulence mechanism of Vibrio anguillarum by Milton D. L. (1992)
  33. Milton , D. L. , R. O'Toole , P. Hörstedt , and H. Wolf-Watz . 1996 . Flagellin A is essential for the virulence of Vibrio anguillarum . J. Bacteriol. 178 : 1310 - 1319 . (10.1128/jb.178.5.1310-1319.1996) / J. Bacteriol. / Flagellin A is essential for the virulence of Vibrio anguillarum by Milton D. L. (1996)
  34. Moré , M. I. , L. D. Finger , J. L. Stryker , C. Fuqua , A. Eberhard , and S. C. Winans . 1996 . Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates . Science 272 : 1655 - 1658 . (10.1126/science.272.5268.1655) / Science / Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates by Moré M. I. (1996)
  35. Norqvist , A. , Å. Hagström, and H. Wolf-Watz . 1989 . Protection of rainbow trout against vibriosis and furunculosis by the use of attenuated strains of Vibrio anguillarum . Appl. Environ. Microbiol. 55 : 1400 - 1405 . (10.1128/aem.55.6.1400-1405.1989) / Appl. Environ. Microbiol. / Protection of rainbow trout against vibriosis and furunculosis by the use of attenuated strains of Vibrio anguillarum by Norqvist A. (1989)
  36. Norqvist , A. , and H. Wolf-Watz . 1993 . Characterization of a novel chromosomal virulence locus involved in expression of a major surface flagellar sheath antigen of the fish pathogen Vibrio anguillarum . Infect. Immun. 61 : 2434 - 2444 . (10.1128/IAI.61.6.2434-2444.1993) / Infect. Immun. / Characterization of a novel chromosomal virulence locus involved in expression of a major surface flagellar sheath antigen of the fish pathogen Vibrio anguillarum by Norqvist A. (1993)
  37. O'Toole , R. , D. L. Milton , and H. Wolf-Watz . 1996 . Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum . Mol. Microbiol. 19 : 625 - 637 . (10.1046/j.1365-2958.1996.412927.x) / Mol. Microbiol. / Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum by O'Toole R. (1996)
  38. Passador , L. , J. M. Cook , M. J. Gambello , L. Rust , and B. H. Iglewski . 1993 . Expression of Pseudomonas aeruginosa virulence genes requires cell-cell communication . Science 260 : 1127 - 1130 . (10.1126/science.8493556) / Science / Expression of Pseudomonas aeruginosa virulence genes requires cell-cell communication by Passador L. (1993)
  39. Pearson , J. P. , K. M. Gray , L. Passador , K. D. Tucker , A. Eberhard , B. H. Iglewski , and E. P. Greenberg . 1994 . Structure of the autoinducer required for expression of the Pseudomonas aeruginosa virulence genes . Proc. Natl. Acad. Sci. USA 91 : 197 - 201 . (10.1073/pnas.91.1.197) / Proc. Natl. Acad. Sci. USA / Structure of the autoinducer required for expression of the Pseudomonas aeruginosa virulence genes by Pearson J. P. (1994)
  40. Pearson , J. P. , L. Passador , B. H. Iglewski , and E. P. Greenberg . 1995 . A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa . Proc. Natl. Acad. Sci. USA 92 : 1490 - 1494 . (10.1073/pnas.92.5.1490) / Proc. Natl. Acad. Sci. USA / A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa by Pearson J. P. (1995)
  41. Piper , K. R. , S. Beck von Bodman , and S. K. Farrand . 1993 . Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction . Nature 362 : 448 - 450 . (10.1038/362448a0) / Nature / Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction by Piper K. R. (1993)
  42. Pirhonen , M. , D. Flego , R. Heikinheimo , and E. T. Palva . 1993 . A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in Erwinia carotovora . EMBO J. 12 : 2467 - 2476 . (10.1002/j.1460-2075.1993.tb05901.x) / EMBO J. / A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in Erwinia carotovora by Pirhonen M. (1993)
  43. Postle , K. , and R. F. Good . 1985 . A bidirectional rho-independent transcription terminator between the E. coli tonB gene and an opposing gene . Cell 41 : 577 - 585 . (10.1016/S0092-8674(85)80030-1) / Cell / A bidirectional rho-independent transcription terminator between the E. coli tonB gene and an opposing gene by Postle K. (1985)
  44. Reed , L. J. , and J. Muench . 1938 . A simple method of estimating fifty percent endpoints . Am. J. Hyg. 27 : 493 - 497 . / Am. J. Hyg. / A simple method of estimating fifty percent endpoints by Reed L. J. (1938)
  45. Salmond , G. P. C. , B. W. Bycroft , G. S. A. B. Stewart , and P. Williams . 1995 . The bacterial `enigma`: cracking the code of cell-cell communication . Mol. Microbiol. 16 : 615 - 624 . (10.1111/j.1365-2958.1995.tb02424.x) / Mol. Microbiol. / The bacterial `enigma`: cracking the code of cell-cell communication by Salmond G. P. C. (1995)
  46. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  47. Schaefer , A. L. , D. L. Val , B. L. Hanzelka , J. E. Cronan , Jr. , and E. P. Greenberg . 1996 . Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein . Proc. Natl. Acad. Sci. USA 93 : 9505 - 9509 . (10.1073/pnas.93.18.9505) / Proc. Natl. Acad. Sci. USA / Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein by Schaefer A. L. (1996)
  48. Schripsen , J. , K. E. E. de Rudder , T. B. van Vliet , P. P. Lankhorst , E. de Vroom , J. W. Kijne , and A. A. van Brussel . 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-transcription factors . J. Bacteriol. 178 : 366 - 371 . (10.1128/jb.178.2.366-371.1996) / J. Bacteriol. / Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-L-homoserine lactone molecules known as autoinducers and as quorum sensing co-transcription factors by Schripsen J. (1996)
  49. Seed , P. C. , L. Passador , and B. H. Iglewski . 1995 . Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas aeruginosa autoinducer PAI: an autoinduction regulatory hierarchy . J. Bacteriol. 177 : 654 - 659 . (10.1128/jb.177.3.654-659.1995) / J. Bacteriol. / Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas aeruginosa autoinducer PAI: an autoinduction regulatory hierarchy by Seed P. C. (1995)
  50. Simon , R. , U. Priefer , and A. Pühler . 1983 . A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria . Bio/Technology 1 : 787 - 796 . (10.1038/nbt1183-784) / Bio/Technology / A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria by Simon R. (1983)
  51. Stevens , A. M. , K. M. Dolan , and E. P. Greenberg . 1994 . Synergistic binding of the Vibrio fischeri transcriptional activator domain and RNA polymerase to the lux promoter region . Proc. Natl. Acad. Sci. USA 91 : 12619 - 12623 . (10.1073/pnas.91.26.12619) / Proc. Natl. Acad. Sci. USA / Synergistic binding of the Vibrio fischeri transcriptional activator domain and RNA polymerase to the lux promoter region by Stevens A. M. (1994)
  52. Swift , S. , M. K. Winson , P. F. Chan , N. J. Bainton , M. Birdsall , P. J. Reeves , C. E. D. Rees , S. R. Chhabra , P. J. Hill , J. P. Throup , B. W. Bycroft , G. P. C. Salmond , P. Williams , and G. S. A. B. Stewart . 1993 . A novel strategy for the isolation of luxI homogues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria . Mol. Microbiol. 10 : 511 - 520 . (10.1111/j.1365-2958.1993.tb00923.x) / Mol. Microbiol. / A novel strategy for the isolation of luxI homogues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria by Swift S. (1993)
  53. Throup , J. P. , M. Camara , G. S. Briggs , M. K. Winson , S. R. Chhabra , B. W. Bycroft , P. Williams , and G. S. A. B. Stewart . 1995 . Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules . Mol. Microbiol. 17 : 345 - 356 . (10.1111/j.1365-2958.1995.mmi_17020345.x) / Mol. Microbiol. / Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules by Throup J. P. (1995)
  54. Trust , T. J. , I. D. Courtice , A. G. Khouri , J. H. Crosa , and M. H. Schiewe . 1981 . Serum resistance and haemagglutination ability of marine vibrios pathogenic to fish . Infect. Immun. 34 : 702 - 707 . (10.1128/IAI.34.3.702-707.1981) / Infect. Immun. / Serum resistance and haemagglutination ability of marine vibrios pathogenic to fish by Trust T. J. (1981)
  55. Williams , P. , N. J. Bainton , S. Swift , S. R. Chhabra , M. K. Winson , G. S. A. B. Stewart , G. P. C. Salmond , and B. W. Bycroft . 1992 . Smallmolecule mediated density-dependent control of gene expression in prokaryotes: bioluminescence and the biosynthesis of carbapenem antibiotics . FEMS Microbiol. Lett. 100 : 161 - 168 . (10.1111/j.1574-6968.1992.tb05698.x) / FEMS Microbiol. Lett. / Smallmolecule mediated density-dependent control of gene expression in prokaryotes: bioluminescence and the biosynthesis of carbapenem antibiotics by Williams P. (1992)
  56. Winson , M. K. , M. Camara , A. Latifi , M. Foglino , S. R. Chhabra , M. Daykin , M. Bally , V. Chapon , G. P. C. Salmond , B. W. Bycroft , A. Lazdunski , G. S. A. B. Stewart , and P. Williams . 1995 . Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa . Proc. Natl. Acad. Sci. USA 92 : 9427 - 9431 . (10.1073/pnas.92.20.9427) / Proc. Natl. Acad. Sci. USA / Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa by Winson M. K. (1995)
  57. Wirth , R. , A. Muscholi , and G. Wanner . 1996 . The role of pheromones in bacterial interactions . Trends Microbiol. 4 : 96 - 102 . (10.1016/0966-842X(96)81525-3) / Trends Microbiol. / The role of pheromones in bacterial interactions by Wirth R. (1996)
  58. Wood , D. W. , and L. S. Pierson III . 1996 . The phzI gene of Pseudomonas aureofaciens 30-84 is responsible for the production of a diffusible signal required for phenazine antibiotic production . Gene 168 : 49 - 53 . (10.1016/0378-1119(95)00754-7) / Gene / The phzI gene of Pseudomonas aureofaciens 30-84 is responsible for the production of a diffusible signal required for phenazine antibiotic production by Wood D. W. (1996)
  59. Zhang , L. , P. J. Murphy , A. Kerr , and M. E. Tate . 1993 . Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones . Nature 362 : 446 - 448 . (10.1038/362446a0) / Nature / Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones by Zhang L. (1993)
Dates
Type When
Created 8 years, 9 months ago (Nov. 14, 2016, 5:39 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 2:10 p.m.)
Indexed 4 weeks, 1 day ago (Aug. 5, 2025, 8:48 a.m.)
Issued 28 years, 4 months ago (May 1, 1997)
Published 28 years, 4 months ago (May 1, 1997)
Published Print 28 years, 4 months ago (May 1, 1997)
Funders 0

None

@article{Milton_1997, title={Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone}, volume={179}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.179.9.3004-3012.1997}, DOI={10.1128/jb.179.9.3004-3012.1997}, number={9}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Milton, D L and Hardman, A and Camara, M and Chhabra, S R and Bycroft, B W and Stewart, G S and Williams, P}, year={1997}, month=may, pages={3004–3012} }