The evolution of bacterial LuxI and LuxR quorum sensing regulators Free

Abstract

Quorum sensing is a widespread form of bacterial communication in which individual cells produce and respond to specific -acyl homoserine lactone signal metabolites. The different autoinducer synthases that generate these signals and the receptor/activator proteins that mediate the cell’s response to them constitute evolutionarily conserved families of regulatory proteins known as the LuxI and LuxR families, respectively. We have performed a phylogenetic analysis of 76 individual LuxI and LuxR homologues present in diverse members of the Gram-negative . The results were consistent with an early origin for these regulators during the evolution of the , with functional pairs of and genes possibly coevolving as regulatory cassettes. In many cases, specific LuxI and LuxR family members appeared to have been inherited horizontally. In particular, those species containing multiple LuxI and/or LuxR homologues usually appeared to have obtained each individual homologue or functional pair of homologues from an independent source. Because multiple homologues interact to form regulatory cascades, this finding suggests that hierarchical signalling pathways can potentially evolve by the sequential integration of pre-existing regulatory circuits acquired from diverse sources.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-8-2379
2001-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/8/1472379a.html?itemId=/content/journal/micro/10.1099/00221287-147-8-2379&mimeType=html&fmt=ahah

References

  1. Ahmer B. M., Timmers C. D., Valentine P. J., Heffron F., van Reeuwijk J. 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]
  2. Blattner F. R., Bloch C. A., Plunkett G. III 14 other authors 1997; The complete genome sequence of Escherichia coli K12. Science 277:1453–1474 [CrossRef]
    [Google Scholar]
  3. Cox A. R. J., Thompson N. R., Bycroft B., Stewart G. S. A. B., Williams P., Salmond G. P. C. 1998; A pheromone-independent CarR protein controls carbapenem antibiotic synthesis in the opportunistic human pathogen Serratia marcescens. . Microbiology 144:201–209 [CrossRef]
    [Google Scholar]
  4. Fuqua C., Eberhard A. 1999; Signal generation in autoinduction systems: synthesis of acylated homoserine lactones by LuxI-type proteins. In Cell–Cell Signaling in Bacteria pp 211–230 Edited by Dunny G. M., Winans S. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  5. Greenberg E. P. 2000; Acyl-homoserine lactone quorum sensing in bacteria. J Microbiol 38:117–121
    [Google Scholar]
  6. Henikoff S., Wallace J. C., Brown J. P. 1990; Finding protein similarities with nucleotide sequence databases. Methods Enzymol 183:111–132
    [Google Scholar]
  7. Higgins D. G., Sharp P. M. 1989; Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS 5:151–153
    [Google Scholar]
  8. Holden M. T. G., McGowan S. J., Bycroft B. W., Stewart G. S. A. B., Williams P., Salmond G. P. C. 1998; Cryptic carbapenem antibiotic production genes are widespread in Erwinia carotovora : facile trans activation by the carR transcriptional regulator. Microbiology 144:1495–1508 [CrossRef]
    [Google Scholar]
  9. Jain R., Rivera M. C., Lake J. A. 1999; Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 96:3801–3806 [CrossRef]
    [Google Scholar]
  10. Kishino H., Hasegawa M. 1989; Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Homonoidea. . J Mol Evol 29:170–179 [CrossRef]
    [Google Scholar]
  11. Kumar S., Tamura K., Nei M. 1994; mega: molecular evolutionary genetics analysis software for microcomputers. Comput Applic Biosci 10:189–191
    [Google Scholar]
  12. 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 21:1137–1146 [CrossRef]
    [Google Scholar]
  13. Lawrence J. G. 1997; Selfish operons and speciation by gene transfer. Trends Microbiol 5:355–359 [CrossRef]
    [Google Scholar]
  14. Lawrence J. G., Ochman H. 1998; Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95:9413–9417 [CrossRef]
    [Google Scholar]
  15. McGowan S., Sebaihia M., Jones S. 7 other authors 1995; Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator. Microbiology 141:541–550 [CrossRef]
    [Google Scholar]
  16. Nicholas K. B., Nicholas H. B. Jr 1997 GeneDoc: a Tool for Editing and Annotating Multiple Sequence Alignments http://www.psc.edu/biomed/genedoc Pittsburgh, PA: Pittsburgh Supercomputing Center;
    [Google Scholar]
  17. Oger P., Kim K.-S., Sackett R. L., Piper K. R., Farrand S. K. 1998; Octopine-type Ti plasmids code for a mannopine-inducible dominant-negative allele of traR , the quorum-sensing activator that regulates Ti plasmid conjugal transfer. Mol Microbiol 27:277–288 [CrossRef]
    [Google Scholar]
  18. Parsek M. R., Greenberg E. P. 2000; Acyl-homoserine lactone quorum sensing in Gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci USA 97:8789–8793 [CrossRef]
    [Google Scholar]
  19. Pesci E. C., Pearson J. P., Seed P. C., Iglewski B. H. 1997; Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. . J Bacteriol 179:3127–3132
    [Google Scholar]
  20. Pirhonen M., Flego D., Heikinheimo R., Palva E. T. 1993; A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. . EMBO J 12:2467–2476
    [Google Scholar]
  21. Rodelas B., Lithgow J. K., Wisniewski-Dye F., Hardman A., Wilkinson A., Economou A., Williams P., Downie J. A. 1999; Analysis of quorum-sensing-dependent control of rhizosphere-expressed ( rhi ) genes in Rhizobium leguminosarum bv. viciae. J Bacteriol 181:3816–3823
    [Google Scholar]
  22. Shapiro J. A. 1998; Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104 [CrossRef]
    [Google Scholar]
  23. Sitnikov D. M., Schineller J. B., Baldwin T. O. 1996; Control of cell division in Escherichia coli : regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction. Proc Natl Acad Sci USA 93:336–341 [CrossRef]
    [Google Scholar]
  24. Slock J., VanRiet D., Kolibachuk D., Greenberg E. P. 1990; Critical regions of the Vibrio fischeri LuxR protein defined by mutational analysis. J Bacteriol 172:3974–3979
    [Google Scholar]
  25. Stevens A. M., Greenberg E. P. 1999; Transcriptional activation by LuxR. In Cell–Cell Signaling in Bacteria pp 231–242 Edited by Dunny G. M., Winans S. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  26. Surette M. G., Bassler B. L. 1998; Quorum sensing in Escherichia coli and Salmonella typhimurium. . Proc Natl Acad Sci USA 95:7046–7050 [CrossRef]
    [Google Scholar]
  27. Surette M. G., Bassler B. L. 1999; Regulation of autoinducer production in Salmonella typhimurium. . Mol Microbiol 31:585–595 [CrossRef]
    [Google Scholar]
  28. Surette M. G., Miller M. B., Bassler B. L. 1999; Quorum sensing in Escherichia coli, Salmonella typhimurium , and Vibrio harveyi : a new family of genes responsible for autoinducer production. Proc Natl Acad Sci USA 96:1639–1644 [CrossRef]
    [Google Scholar]
  29. Swift S., Williams P., Stewart G. S. A. B. 1999; N -Acyl homoserine lactones and quorum sensing in proteobacteria. In Cell–Cell Signaling in Bacteria pp 291–313 Edited by Dunny G. M., Winans S. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  30. Swofford D. L. 2000 paup *. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  31. Templeton A. R. 1983; Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244 [CrossRef]
    [Google Scholar]
  32. Thomson N. R., Crow M. A., McGowan S. J., Cox A., Salmond G. P. C. 2000; Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36:539–556
    [Google Scholar]
  33. Van de Peer Y., Caers A., De Rijk P., De Wachter R. 1998; Database on the structure of small ribosomal subunit RNA. Nucleic Acids Res 26:179–182 [CrossRef]
    [Google Scholar]
  34. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
    [Google Scholar]
  35. Zhu J., Winans S. C. 1998; Activity of the quorum-sensing regulator TraR of Agrobacterium tumefaciens is inhibited by a truncated, dominant-defective TraR-like protein. Mol Microbiol 27:289–297 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-8-2379
Loading
/content/journal/micro/10.1099/00221287-147-8-2379
Loading

Data & Media loading...

Most cited Most Cited RSS feed