sinI- and expR-Dependent quorum sensing in Sinorhizobium meliloti

Journal of Bacteriology

Volumn 187, Issue 23, 2005, Pages 7931-7944

  Gao, Mengsheng ^a   Chen, Hancai ^b   Eberhard, Anatol ^c   Gronquist, Matthew R ^d   Robinson, Jayne B ^e   Rolfe, Barry G ^b   Bauer, Wolfgang D ^a,f  

^a OHIO STATE UNIVERSITY   (United States)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c Department of Obstetrics Gynecology   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

^e UNIVERSITY OF DAYTON   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGIE PROTEIN; BETA GLUCURONIDASE; EXPE6 PROTEIN; EXPR SYNTHASE; GOR PROTEIN; HOMOSERINE; IDHA PROTEIN; LACTONE; LEUC PROTEIN; MOCB PROTEIN; N ACYL HOMOSERINE LACTONE; PCKA PROTEIN; PROTEIN; PROTEOME; SINI SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; DELETION MUTANT; GAS CHROMATOGRAPHY; GENE DISRUPTION; GENE EXPRESSION REGULATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MEDICAGO; MICROBIAL POPULATION DYNAMICS; NITROGEN FIXATION; NODULATION; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; QUORUM SENSING; REPORTER GENE; SINORHIZOBIUM MELILOTI; SYMBIONT; TANDEM MASS SPECTROMETRY; THIN LAYER CHROMATOGRAPHY;

4-BUTYROLACTONE; BACTERIAL PROTEINS; CHROMATOGRAPHY, THIN LAYER; GENES, BACTERIAL; GENES, REPORTER; GLUCURONIDASE; LOCOMOTION; MEDICAGO; MUTATION; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

BACTERIA (MICROORGANISMS); MEDICAGO; MEDICAGO TRUNCATULA; SINORHIZOBIUM MELILOTI;

EID: 28044434851     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.23.7931-7944.2005     Document Type: Article

References (81)

1. Arevalo-Ferro, C., M. Hentzer, G. Reil, A. Gorg, S. Kjelleberg, M. Givskov, K. Riedel, and L. Eberl. 2003. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ. Microbiol. 5:1350-1369.
2. Barrick, J. E., K. A. Corbino, W. C. Winkler, A. Nahvi, M. Mandal, J. Collins, M. Lee, A. Roth, N. Sudarsan, I. Jona, J. K. Wickiser, and R. R. Breaker. 2004. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc. Natl. Acad. Sci. USA 101:6421-6426.
3. Bauer, W. D., and U. Mathesius. 2004. Plant responses to bacterial quorum sensing signals. Curr. Opin. Plant Biol. 7:429-433.
4. Beatson, S. A., C. B. Whitchurch, A. B. Semmler, and J. S. Mattick. 2002. Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J. Bacteriol. 184:3598-3604.
5. Becker, A., S. Ruberg, H. Kuster, A. A. Roxlau, M. Keller, T. Ivashina, H. P. Cheng, G. C. Walker, and A. Puhler. 1997. The 32-kilobase exp gene cluster of Rhizobium meliloti directing the biosynthesis of galactoglucan: genetic organization and properties of the encoded gene products. J. Bacteriol. 179:1375-1384.
6. Bhuvaneswari, T. V., A. Bhagwat, and W. D. Bauer. 1981. Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Plant Physiol. 68:1144-1149.
7. Caetano-Anolles, G., B. Wrobel, and W. D. Bauer. 1992. Growth and movement of spot inoculated Rhizobium meliloti on the root surface of alfalfa. Plant Physiol. 98:1181-1189.
8. Chen, H., J. Higgins, E. Kondorosi, A. Kondorosi, M. A. Djordjevic, J. J. Weinman, and B. G. Rolfe. 2000. Identification of nolR-regulated proteins in Sinorhizobium meliloti using proteome analysis. Electrophoresis 21:3823-3832.
9. Chen, H., J. Higgins, I. J. Oresnik, M. F. Hynes, S. Natera, M. A. Djordjevic, J. J. Weinman, and B. G. Rolfe. 2000. Proteome analysis demonstrates complex replicon and luteolin interactions in pSyma-cured derivatives of Sinorhizobium meliloti strain 2011. Electrophoresis 21:3833-3842.
10. Chen, H., M. Teplitski, M. Gao, J. B. Robinson, B. G. Rolfe, and W. D. Bauer. 2003. Proteomic analysis of wild-type Sinorhizobium meliloti responses to N-acyl homoserine lactone quorum-sensing signals and the transition to stationary phase. J. Bacteriol. 185:5029-5036.
11. Daniels, R., J. Vanderleyden, and J. Michiels. 2004. Quorum sensing and swarming migration in bacteria. FEMS Microbiol. Rev. 28:261-289.
12. Degrassi, G., C. Aguilar, M. Bosco, S. Zahariev, S. Pongor, and V. Venturi. 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.
13. Dickstein, R., D. C. Scheirer, W. H. Fowle, and F. M. Ausubel. 1991. Nodules elicited by Rhizobium meliloti heme mutants are arrested at an early stage of development. Mol. Gen. Genet. 230:423-432.
14. +-dependent malic enzymes of Rhizobium (Sinorhizobium) meliloti and differential expression of their genes in nitrogen-fixing bacteroids. Microbiology 143:489-498.
15. Eberl, L., M. K. Winson, C. Sternberg, G. S. Stewart, G. Christiansen, S. R. Chhabra, B. Bycroft, P. Williams, S. Molin, and M. Givskov. 1996. Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20:127-136.
16. Fuqua, C., M. R. Parsek, and E. P. Greenberg. 2001. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35:439-468.
17. Gage, D. J. 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol Rev. 68:280-300.
18. Galbraith, M. P., S. F. Feng, J. Borneman, E. W. Triplett, F. J. de Bruijn, and S. Rossbach. 1998. A functional myo-inositol catabolism pathway is essential for rhizopine utilization by Sinorhizobium meliloti. Microbiology 144:2915-2924.
19. Galibert, F., T. M. Finan, S. R. Long, R. A. Puhle, P. Abola, F. Ampe, F. Barloy-Hubler, M. J. Barnett, A. Becker, P. Boistard, G. Bothe, M. Boutry, L. Bowser, J. Buhrmester, E. Cadieu, D. Capela, P. Chain, A. Cowie, R. W. Davis, S. Dreano, N. A. Federspiel, R. F. Fisher, S. Gloux, T. Godrie, A. Goffeau, B. Golding, J. Gouzy, M. Gurjal, I. Hernandez-Lucas, A. Hong, L. Huizar, R. W. Hyman, T. Jones, D. Kahn, M. L. Kahn, S. Kalman, D. H. Keating, E. Kiss, C. Komp, V. Lelaure, D. Masuy, C. Palm, M. C. Peck, T. M. Pohl, D. Portetelle, B. Purnelle, U. Ramsperger, R. Surzycki, P. Thebault, M. Vandenbol, F. J. Verholter, R. S. Weidne, D. H. Wells, K. Wong, K. C. Yeh, and J. Batut. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
20. Gao, M., M. Teplilski, J. B. Robinson, and W. D. Bauer. 2003. Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol. Plant-Microbe Interact. 16:827-834.
21. Glazebrook, J., A. Ichige, and G. C. Walker. 1996. Genetic analysis of Rhizobium meliloti bacA-phoA fusion results in identification of degP: two loci required for symbiosis are closely linked to degP. J. Bacteriol. 178:745-752.
22. Gonzalez, J. E., B. L. Reuhs, and G. C. Walker. 1996. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc. Natl. Acad. Sci. USA 93:8636-8641.
23. Guerreiro, N., M. A. Djordjevic, and B. G. Rolfe. 1999. Proteome analysis of the model microsymbiont Sinorhizobium meliloti: isolation and characterisation of novel proteins. Electrophoresis 20:818-825.
24. Harrison, J., A. Jamet, C. I. Muglia, G. Van de Sype, O. M. Aguilar, A. Puppo, and P. Frendo. 2005. Glutathione plays a fundamental role in growth and symbiotic capacity of Sinorhizobium meliloti. J. Bacteriol. 187:168-174.
25. Hassani, R., C. K. Prasad, K. E. Vineetha, N. Vij, P. Singh, R. Sud, S. Yadav, and G. S. Randhawa. 2002. Symbiotic characterization of isoleucine+valine and leucine auxotrophs of Sinorhizobium meliloti. Indian J. Exp. Biol. 40:1110-1120.
26. Hentzer, M., H. Wu, J. B. Andersen, K. Riedel, T. B. Rasmussen, N. Bagge, N. Kumar, M. A. Schembri, Z. Song, P. Kristoffersen, M. Manefield, J. W. Costerton, S. Molin, L. Eberl, P. Steinberg, S. Kjelleberg, N. Hoiby, and M. Givskov. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22:3803-3815.
27. Hoang, H. H., A. Becker, and J. E. Gonzalez. 2004. The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium meliloti gene expression. J. Bacteriol. 186:5460-5472.
28. Holden, M. T., S. Ram Chhabra, R. de Nys, P. Stead, N. J. Bainton, P. J. Hill, M. Manefield, N. Kumar, M. Laballe, D. England, S. Rice, M. Givskov, G. P. Salmond, G. S. Stewart, B. W. Bycroft, S. Kjelleberg, and P. Williams. 1999. Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol. Microbiol. 33:1254-1266.
29. Hubber, A., A. C. Vergunst, J. T. Sullivan, P. J. Hooykaas, and C. W. Ronson. 2004. Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol. Microbiol. 54:561-574.
30. Ibrahim, Y. M., A. R. Kerr, J. McCluskey, and T. J. Mitchell. 2004. Control of virulence by the two-component system CiaR/H is mediated via HtrA, a major virulence factor of Streptococcus pneumoniae. J. Bacteriol. 186:5258-5266.
31. Jensen, H. L. 1942. Nitrogen fixation in leguminous plants. I. General characters of root nodule bacteria isolated from species of Medicago and Trifolium in Australia. Proc. Linn. Soc. N. S. W. 66:98-108.
32. Jensen, J. B., N. K. Peters, and T. V. Bhuvaneswari. 2002. Redundancy in periplasmic binding protein-dependent transport systems for trehalose, sucrose, and maltose in Sinorhizobium meliloti. J. Bacteriol. 184:2978-2986.
33. Jiang, G., A. H. Krishnan, Y. W. Kim, T. J. Wacek, and H. B. Krishnan. 2001. A functional myo-inositol dehydrogenase gene is required for efficient nitrogen fixation and competitiveness of Sinorhizobium fredii USDA191 to nodulate soybean (Glycine max [L.] Merr.). J. Bacteriol. 183:2595-2604.
34. Laue, B. E., Y. Jiang, S. R. Chhabra, S. Jacob, G. S. Stewart, A. Hardman, J. A. Downie, F. O'Gara, and P. Williams. 2000. The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146(Pt. 10):2469-2480.
35. Ledgham, F., I. Ventre, C. Soscia, M. Foglino, J. N. Sturgis, and A. Lazdunski. 2003. Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol. Microbiol. 48:199-210.
36. Loh, J., E. A. Pierson, L. S. Pierson III, G. Stacey, and A. Chatterjee. 2002. Quorum sensing in plant-associated bacteria. Curr. Opin. Plant Biol. 5:285-290.
37. Long, S. 1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885-1898.
38. Mandal, M., M. Lee, J. E. Barrick, Z. Weinberg, G. M. Emilsson, W. L. Ruzzo, and R. R. Breaker. 2004. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306:275-279.
39. Marketon, M. M., S. A. Glenn, A. Eberhard, and J. E. Gonzalez. 2003. Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J. Bacteriol. 185:325-331.
40. Marketon, M. M., and J. E. Gonzalez. 2002b. Identification of two quorum-sensing systems in Sinorhizobium meliloti. J. Bacteriology 184:3466-3475.
41. Marketon, M. M., M. R. Gronquist, A. Eberhard, and J. E. Gonzalez. 2002a. Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J. Bacteriol. 184:5686-5695.
42. Mathesius, U., S. Mulders, M. Gao, M. Teplitski, G. Caetano-Anolles, B. G. Rolfe, and W. D. Bauer. 2003. Extensive and specific responses of a eukaryote to bacterial quorum sensing signals. Proc. Natl. Acad. Sci. USA 100:1444-1449.
43. Matthysse, A. G., H. A. Yarnall, and N. Young. 1996. Requirement for genes with homology to ABC transport systems for attachment and virulence of Agrobacterium tumefaciens. J. Bacteriol. 178:5302-5308.
44. Meade, H. M., and E. R. Signer. 1977. Genetic mapping of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 74:2076-2078.
45. Murphy, P. J., and C. P. Saint. 1992. Rhizopines in the legume-Rhizobium symbiosis, p. 377-390. In D. P. S. Verma (ed.), Molecular signals in plant-microbe communication. CRC Press, Inc., Boca Raton, Fla.
46. Murphy, P. J., W. Wexler, W. Grzemski, J. P. Rao, and D. Gordon. 1995. Rhizopines-their role in symbiosis and competition. Soil Biol. Biochem. 27:525-529.
47. 32 homolog (RpoH) plays a major role in the heat shock response of Agrobacterium tumefaciens. J. Bacteriol. 183:5302-5310.
48. Natera, S. H. A., N. Guerreiro, and M. A. Djordjevic. 2000. Proteome analysis of differentially displayed proteins as a tool for the investigation of symbiosis. Mol. Plant-Microbe. Interact. 13:995-1009.
49. Neuhoff, V., N. Arold, D. Taube, and W. Ehrhardt. 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255-262.
50. Nudler, E., and A. S. Mironov. 2004. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 29:11-17.
51. Oke, V., and S. R. Long. 1999. Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol. Microbiol. 32:837-849.
52. Oke, V., B. G. Rushing, E. J. Fisher, M. Moghadam-Tabrizi, and S. R. Long. 2001. Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium meliloti. Microbiology 147:2399-2408.
53. Osteras, M., B. T. Driscoll, and T. M. Finan. 1995. Molecular and expression analysis of the Rhizobium meliloti phosphoenolpyruvate carboxykinase (pckA) gene. J. Bacteriol. 177:1452-1460.
54. Osteras, M., T. M. Finan, and J. Stanley. 1991. Site-directed mutagenesis and DNA sequence of pckA of Rhizobium NGR234, encoding phosphoenol-pyruvate carboxykinase: gluconeogenesis and host-dependent symbiotic phenotype. Mol. Gen. Genet. 230:257-269.
55. Pellock, B. J., M. Teplitski, R. P. Boinay, W. D. Bauer, and G. C. Walker. 2002. A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J. Bacteriol. 184:5067-5076.
56. Quandt, J., and M. F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21.
57. Reeve, W. G., R. P. Tiwari, N. Guerreiro, J. Stubbs, M. J. Dilworth, A. R. Glenn, B. G. Rolfe, M. A. Djordjevic, and J. G. Howieson. 2004. Probing for pH-regulated proteins in Sinorhizobium medicae using proteomic analysis. J. Mol. Microbiol. Biotechnol. 7:140-147.
58. Reimmann, C., N. Ginet, L. Michel, C. Keel, P. Michaux, V. Krishnapillai, M. Zala, K. Heurlier, K. Triandafillu, H. Harms, G. Defago, and D. Haas. 2002. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148:923-932.
59. Reuber, T. L., A. Urzainqui, J. Glazebrook, J. W. Reed, and G. C. Walker. 1995. Rhizobium meliloti exopolysaccharides. Structures, genetic analyses, and symbiotic roles. Ann. N. Y. Acad. Sci. 646:61-68.
60. Rossbach, S., D. A. Kulpa, U. Rossbach, and F. J. de Bruijn. 1994. Molecular and genetic characterization of the rhizopine catabolism (mocABRC) genes of Rhizobium meliloti L5-30. Mol. Gen. Genet. 245:11-24.
61. Schuster, M., C. P. Lostroh, T. Ogi, and E. P. Greenberg. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:2066-2079.
62. Sharypova, L. A., K. Niehaus, H. Scheidle, O. Holst, and A. Becker. 2003. Sinorhizobium meliloti acpXL mutant lacks the C28 hydroxylated fatty acid moiety of lipid A and does not express a slow migrating form of lipopolysaccharide. J. Biol. Chem. 278:12946-12954.
63. Shaw, P. D., G. Ping, S. L. Daly, C. Cha, J. E. Cronan, Jr., K. L. Rinehart, and S. K. Farrand. 1997. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. USA 94:6036-6041.
64. Soto, M. J., M. Fernandez-Pascual, J. Sanjuan, and J. Olivares. 2002. A fadD mutant of Sinorhizobium meliloti shows multicellular swarming migration and is impaired in nodulation efficiency on alfalfa roots. Mol. Microbiol. 43:371-382.
65. Steidle, A., K. Sigl, R. Schuhegger, A. Ihring, M. Schmid, S. Gantner, M. Stoffels, K. Riedel, M. Givskov, A. Hartmann, C. Langebartels, and L. Eberl. 2001. Visualization of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl. Environ. Microbiol. 67:5761-5770.
66. Suess, B., B. Fink, C. Berens, R. Stentz, and W. Hillen. 2004. A theophylline responsive riboswitch based on helix slipping controls gene expression in vivo. Nucleic Acids Res. 32:1610-1614.
67. Teplitski, M., H. Chen, S. Rajamani, M. Gao, M. Merighi, R. T. Sayre, J. B. Robinson, B. G. Rolfe, and W. D. Bauer. 2004. Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol. 134:137-146.
68. Teplitski, M., A. Eberhard, M. Gronquist, M. Gao, J. B. Robinson, and W. D. Bauer. 2003. Chemical identification of N-acyl homoserine lactone quorum sensing signals produced by Sinorhizobium meliloti strains in defined medium. Arch. Microbiol. 180:494-497.
69. Teplitski, M., J. B. Robinson, and W. D. Bauer. 2000. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant-Microbe. Interact. 13:637-648.
70. Tinimers, A. C., E. Soupene, M. C. Auriac, F. de Billy, J. Vasse, P. Boistard, and G. Truchet. 2000. Saprophytic intracellular rhizobia in alfalfa nodules. Mol. Plant-Microbe. Interact. 13:1204-1213.
71. Vasil, M. L. 2003. DNA microarrays in analysis of quorum sensing: strengths and limitations. J. Bacteriol. 185:2061-2065.
72. Ventre, I., F. Ledgham, V. Prima, A. Lazdunski, M. Foglino, and J. N. Sturgis. 2003. Dimerization of the quorum sensing regulator RhlR: development of a method using EGFP fluorescence anisotropy. Mol. Microbiol. 48:187-198.
73. Visick, K. L., and E. G. Ruby. 1999. The emergent properties of quorum-sensing: consequences to bacteria of autoinducer signalling in their natural environment, p. 333-352. In G. M. Dunny and S. Winans (ed.), Cell-cell signaling in bacteria. ASM Press, Washington, D.C.
74. von Bodman, S. B., W. D. Bauer, and D. L. Coplin. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Plant Pathol. 41:455-482.
75. Wagner, V. E., D. Bushnell, L. Passador, A. I. Brooks, and B. H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185:2080-2095.
76. Weiller, G. F., M. J. Djordjevic, G. Caraux, H. Chen, and J. J. Weinman. 2001. A specialised proteomic database for comparing matrix-assisted laser desorption/ionization-time of flight mass spectrometry data of tryptic peptides with corresponding sequence database segments. Proteomics 1:1489-1494.
77. Whitehead, N. A., A. M. Barnard, H. Slater, N. J. Simpson, and G. P. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365-404.
78. Willis, L. B., and G. C. Walker. 1999. A novel Sinorhizobium meliloti operon encodes an α-glucosidase and a periplasmic-binding-protein- dependent transport system for α-glucosides. J. Bacteriol. 181:4176-4184.
79. Winston M. K., S. Swift, L. Fish, J. P. Throup, F. Jorgensen, S. R. Chhabra, B. W. Bycroft, P. Williams, and G. S. Stewart. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163:185-192.
80. Winzer, K., and P. Williams. 2001. Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria. Int. J. Med. Microbiol. 291:131-143.
81. Yates, E. A., B. Philipp, C. Buckley, S. Atkinson, S. R. Chhabra, R. E. Sockett, M. Goldner, Y. Dessaux, M. Camara, H. Smith, and P. Williams. 2002. N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun. 70:5635-5646.