1887

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
2020-03-28
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 Bacteriol180:1185–1193
    [Google Scholar]
  2. Blattner F. R., Bloch C. A., Plunkett G. III. 14 other authors 1997; The complete genome sequence of Escherichia coli K12. Science277:1453–1474[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 pp211–230 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 Microbiol38:117–121
    [Google Scholar]
  6. Henikoff S., Wallace J. C., Brown J. P.. 1990; Finding protein similarities with nucleotide sequence databases. Methods Enzymol183:111–132
    [Google Scholar]
  7. Higgins D. G., Sharp P. M.. 1989; Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS5:151–153
    [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. Microbiology144:1495–1508[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 USA96:3801–3806[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 Evol29:170–179[CrossRef]
    [Google Scholar]
  11. Kumar S., Tamura K., Nei M.. 1994; mega: molecular evolutionary genetics analysis software for microcomputers. Comput Applic Biosci10:189–191
    [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 Microbiol21:1137–1146[CrossRef]
    [Google Scholar]
  13. Lawrence J. G.. 1997; Selfish operons and speciation by gene transfer. Trends Microbiol5:355–359[CrossRef]
    [Google Scholar]
  14. Lawrence J. G., Ochman H.. 1998; Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA95:9413–9417[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. Microbiology141:541–550[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 Microbiol27:277–288[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 USA97:8789–8793[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 Bacteriol179:3127–3132
    [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 J12:2467–2476
    [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 Bacteriol181:3816–3823
    [Google Scholar]
  22. Shapiro J. A.. 1998; Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol52:81–104[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 USA93:336–341[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 Bacteriol172:3974–3979
    [Google Scholar]
  25. Stevens A. M., Greenberg E. P.. 1999; Transcriptional activation by LuxR. In Cell–Cell Signaling in Bacteria pp231–242 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 USA95:7046–7050[CrossRef]
    [Google Scholar]
  27. Surette M. G., Bassler B. L.. 1999; Regulation of autoinducer production in Salmonella typhimurium. . Mol Microbiol31:585–595[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 USA96:1639–1644[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 pp291–313 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. Evolution37:221–244[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 Microbiol36:539–556
    [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 Res26:179–182[CrossRef]
    [Google Scholar]
  34. Woese C. R.. 1987; Bacterial evolution. Microbiol Rev51:221–271
    [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 Microbiol27:289–297[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 this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error