The Evolutionary History of Quorum-Sensing Systems in Bacteria

Molecular Biology and Evolution

Volumn 21, Issue 5, 2004, Pages 903-913

  Lerat, Emmanuelle ^a   Moran, Nancy A ^a  

^a University of Arizona   (United States)

Author keywords

Evolution; Gene duplication; Gene family; Lateral gene transfer; Phylogenetics; Quorum sensing

Indexed keywords

BACTERIAL PROTEIN; LUXI PROTEIN; RECEPTOR; RIBOSOME RNA; S RIBOSYLHOMOCYSTEINASE; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM; CELL COMMUNICATION; ECOLOGY; EVOLUTION; FIRMICUTES; GENE DUPLICATION; GENE LOSS; GRAM NEGATIVE BACTERIUM; HORIZONTAL GENE TRANSFER; MULTIGENE FAMILY; PHYLOGENY; PSEUDOMONAS AERUGINOSA; QUORUM SENSING SYSTEM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

BACTERIA; BACTERIAL PROTEINS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER TECHNIQUES; GENOME, BACTERIAL; PHYLOGENY; PSEUDOMONAS AERUGINOSA; REPRESSOR PROTEINS; RNA, RIBOSOMAL; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); FIRMICUTES; GAMMAPROTEOBACTERIA; NEGIBACTERIA; PROKARYOTA; PROTEOBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 1942469383     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh097     Document Type: Article

References (51)

1. Ahmer, B. M., J. van Reeuwijk, C. D. Timmers, P. J. Valentine, and F. Heffron. 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.
2. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Andersson, R. A., A. R. Eriksson, R. Heikinheimo, A. Mae, M. Pirhonen, V. Koiv, H. Hyytiainen, A. Tuikkala, and E. T. Palva. 2000. Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expR(Ecc). Mol. Plant Microbe Interact. 13:384-393.
4. Bainton, N. J., P. Stead, S. R. Chhabra, B. W. Bycroft, G. P. Salmond, G. S. Stewart, and P. Williams. 1992. N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288:997-1004.
5. Bassler, B. L., M. Wright, R. E. Showalter, and M. R. Silverman. 1993. Intercellular signaling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9:773-786.
6. Bassler, B. L., M. Wright, and M. R. Silverman. 1994. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13:273-286.
7. Bhattacharyya, A., S. Stilwagen, N. Ivanova et al. (22 co-authors). 2002. Whole-genome comparative analysis of three phytopathogenic Xylella fastidiosa strains. Proc. Natl. Acad. Sci. USA 99:12403-12408.
8. Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, B. A. Rapp, and D. L. Wheeler. 2002. GenBank. Nucleic Acids Res. 25:3389-3402.
9. Bolotin, A., P. Wincker, S. Mauger, O. Jaillon, K. Malarme, J. Weissenbach, S. D. Ehrlich, and S. Sorokin. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11: 731-753.
10. Boucher, Y., C. J. Douday, R. T. Papke, D. A. Walsh, M. E. R. Boudreau, C. L. Nesbø, R. J. Case, and W. F. Doolittle. 2003. Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 37:283-328.
11. Brint, J. M., and D. E. Ohman. 1995. Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J. Bacteriol. 177:7155-7163.
12. Chen, X., S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelczer, B. L. Bassler, and F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545-549.
13. Cox, A. R. J., N.R. Thomson, B. Bycroft, G. S. A. B. Stewart, P. Williams, and G. P. C. Salmond. 1998. A pheromone-independent CarR protein controls carbapenem antibiotic synthesis in the opportunistic human pathogen Serratia marcescens. Microbiology 144:201-209.
14. Dennis, J. J., and G. J. Zylstra. 1998. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl. Environ. Microbiol. 64:2710-2715.
15. Felsenstein, J. 2002. PHYLIP (phylogeny inference package). Version 3.6. Distributed by the author. Department of Genetics, University of Washington, Seattle.
16. 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. 176:2796-3806.
17. Galtier, N., M. Gouy, and C. Gautier. 1996. SeaView and Phylo_win, two graphic tools for sequence alignments and molecular phylogeny. Comput. Appl. Biosci. 12:543-548.
18. Gray, K. M., and J. R. Garey, 2001. The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology 147:2379-2387.
19. Jones, D. T., W. R. Taylor, and J. M. Thorton. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8:275-282.
20. Jones, S., B. Yu, N. J. Bainton, M. Birdsall et al. (13 co-authors). 1993. The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 12:2477-2482.
21. Kanamaru, K., K. Kanamaru, I. Tatsuno, T. Tobe, and C. Sasakawa. 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.
22. Kiratisin, P., K. D. Tucker, and L. Passador. 2002. LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J. Bacteriol. 184:4912-4919.
23. Kleerebezem, M., J. Boekhorst, R. van Kranenburg et al. (20 co-authors). 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. USA 100:1990-1995.
24. Kumar, S., K. Tamura, and M. Nei. 1993. MEGA: molecular eEvolutionary genetics analysis. Version 1.01. The Pennsylvania State University, University Park, Pa.
25. Lerat, E., V. Daubin, and N. A. Moran. 2003. From gene trees to organismal phylogeny in prokaryotes: the case of the γ-Proteobacteria. PLoS Biol. 1:101-109.
26. Lewenza, S., B. Conway, E. P. Greenberg, and P. A. Sokol. 1999. Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J. Bacteriol. 181: 748-756.
27. Lewenza, S., M. B. Visser, and P. A. Sokol. 2002. Interspecies communication between Burkholderia cepacia and Pseudomonas aeruginosa. Can. J. Microbiol. 48:707-716.
28. Lutter, E., S. Lewenza, J. J. Dennis, M. B. Visser, and P. A. Sokol. 2001. Distribution of quorum-sensing genes in the Burkholderia cepacia complex. Infect. Immun. 69:4661-4666.
29. Mavrodi, D. V., V. N. Ksenzenko, R. F. Bonsall, R. J. Cook, A. M. Boronin, and L. S. Thomashow. 1998. A seven-gene locus for synthesis of phenazine-1-carboxylic acid by Pseudomonas fluorescens 2-79. J. Bacteriol. 180:2541-2548.
30. Miller, M. B., and B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165-199.
31. Miller, M. B., K. Skorupski, D. H. Lenz, R. K. Taylor, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303-314.
32. Minogue, T. D., M. Wehland-von Trebra, F. Bernhard, and S. B. von Bodman. 2002. The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol. Microbiol. 44:1625-1635.
33. Mok, K. C., N. S. Wingreen, and B. L. Bassler. 2003. Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J. 22:870-881.
34. Neaslon, K. H., and J. W. Hastings. 1979. Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43:496-518.
35. Ochman, H., J. G. Lawrence, and E. A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304.
36. Ohtani, K., H. Hayashi, and T. Shimizu. 2002. The LuxS gene is involved in cell-cell signaling for toxin production in Clostridium perfringens. Mol. Microbiol. 44:171-179.
37. Passador, L., J. M. Cook, M. J. Gambello, L. Rust, and B. H. Iglewski. 1993. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:1127-1130.
38. 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.
39. Qin, Y., Z.-Q Luo, A. J. Smyth, P. Gao, S Beck von Bodman, and S. K. Farrand. 2000. Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm. EMBO J. 19:5212-5221.
40. Schell, M. A., M. Karmirantzou, B. Snel et al. (12 co-authors). 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. USA 99:14422-14427.
41. Schmidt, H. A., K. Strimmer, M. Vingron, and A. von Haeseler. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502-504.
42. Smith, J. N., and B. M. M. Ahmer. 2003. Detection of other microbial species by Salmonella: expression of the SdiA regulon. J. Bacteriol. 185:1357-1366.
43. Surette, M. G., M. B. Miller, and B. L. Bassler. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for auto-inducer production. Proc. Natl. Acad. Sci. USA 96: 1639-1644.
44. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
45. Thomson, N. R., M. A. Crow, S. J. McGowan, A. Cox, and G. P. Salmond. 2000. Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol. Microbiol. 36:539-556.
46. 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.
47. von Bodman, S. B., W. D. Bauer, and D. L. Coplin. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41:12.1-12.28.
48. Wang, X. D., P. A. de Boer, and L. I. Rothfield. 1991. A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. EMBO J. 10:3363-3372.
49. Welch, M., D. E. Todd, N. A. Whitehead, S. J. McGowan, B. W. Bycroft, and G. P Salmond. 2000. N-acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia. EMBO J. 19:631-641.
50. Whitehead, N. A., A. M. L. Barnard, H. Slater, N. J. L. Simpson, and G. P. C. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365-404.
51. Zhang, Z. and L. S. Pierson 3rd. 2001. A second quorum-sensing system regulates cell surface properties but not phenazine antibiotic production in Pseudomonas aureofaciens. Appl. Environ. Microbiol. 67:4305-4315.