1887

Abstract

-Acylhomoserine lactone (AHL) quorum-sensing (QS) signalling is the best-understood chemical language in proteobacteria. In the last 15 years a large amount of research in several bacterial species has revealed in detail the genetic, molecular and biochemical mechanisms underlying AHL signalling. These studies have revealed the role played by protein pairs of the AHL synthase belonging to the LuxI family and cognate LuxR-family AHL sensor–regulator. Proteobacteria however commonly possess a QS LuxR-family protein for which there is no obvious cognate LuxI synthase; these proteins are found in bacteria which possess a complete AHL QS system(s) as well as in bacteria that do not. Scientists are beginning to address the roles played by these proteins and it is emerging that they could allow bacteria to respond to endogenous and exogenous signals produced by their neighbours. AHL QS research thus far has mainly focused on a cell-density response involving laboratory monoculture studies. Recent findings on the role played by the unpaired LuxR-family proteins highlight the need to address bacterial behaviour and response to signals in mixed communities. Here we review recent progress with respect to these LuxR proteins, which we propose to call LuxR ‘solos’ since they act on their own without the need for a cognate signal generator. Initial investigations have revealed that LuxR solos have diverse roles in bacterial interspecies and interkingdom communication.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.026849-0
2009-05-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/5/1377.html?itemId=/content/journal/micro/10.1099/mic.0.026849-0&mimeType=html&fmt=ahah

References

  1. Ahmer B. M. 2004; Cell-to-cell signalling in Escherichia coli and S almonella enterica . Mol Microbiol 52:933–945
    [Google Scholar]
  2. Bartels F. W., McIntosh M., Fuhrmann A., Metzendorf C., Plattner P., Sewald N., Anselmetti D., Ros R., Becker A. 2007; Effector-stimulated single molecule protein-DNA interactions of a quorum-sensing system in Sinorhizobium meliloti . Biophys J 92:4391–4400
    [Google Scholar]
  3. Bassler B. L. 2002; Small talk. Cell-to-cell communication in bacteria. Cell 109:421–424
    [Google Scholar]
  4. Bassler B. L., Wright M., Showalter R. E., Silverman M. R. 1993; Intercellular signalling in Vibrio harveyi : sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773–786
    [Google Scholar]
  5. Bauer W. D., Mathesius U. 2004; Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 7:429–433
    [Google Scholar]
  6. Case R. J., Labbate M., Kjelleberg S. 2008; AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J 2:345–349
    [Google Scholar]
  7. Chugani S. A., Whiteley M., Lee K. M., D'Argenio D., Manoil C., Greenberg E. P. 2001; QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 98:2752–2757
    [Google Scholar]
  8. Cox A. R., Thomson N. R., Bycroft B., Stewart G. S., Williams P., Salmond G. P. 1998; A pheromone-independent CarR protein controls carbapenem antibiotic synthesis in the opportunistic human pathogen Serratia marcescens . Microbiology 144:201–209
    [Google Scholar]
  9. Danino V. E., Wilkinson A., Edwards A., Downie J. A. 2003; Recipient-induced transfer of the symbiotic plasmid pRL1JI in Rhizobium leguminosarum bv. viciae is regulated by a quorum-sensing relay. Mol Microbiol 50:511–525
    [Google Scholar]
  10. Delrue R. M., Deschamps C., Leonard S., Nijskens C., Danese I., Schaus J. M., Bonnot S., Ferooz J., Tibor A. other authors 2005; A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis . Cell Microbiol 7:1151–1161
    [Google Scholar]
  11. Ferluga S., Venturi V. 2009; OryR is a LuxR-family protein involved in inter-kingdom signaling between pathogenic Xanthomonas oryzae pv. oryzae and rice. J Bacteriol 191:890–897
    [Google Scholar]
  12. Ferluga S., Bigirimana J., Hofte M., Venturi V. 2007; A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol Plant Pathol 8:529–538
    [Google Scholar]
  13. Fuqua C. 2006; The QscR quorum-sensing regulon of Pseudomonas aeruginosa : an orphan claims its identity. J Bacteriol 188:3169–3171
    [Google Scholar]
  14. Fuqua C., Greenberg E. P. 2002; Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695
    [Google Scholar]
  15. Fuqua W. C., Winans S. C., Greenberg E. P. 1994; Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275
    [Google Scholar]
  16. Gilson L., Kuo A., Dunlap P. V. 1995; AinS and a new family of autoinducer synthesis proteins. J Bacteriol 177:6946–6951
    [Google Scholar]
  17. Glenn S. A., Gurich N., Feeney M. A., Gonzalez J. E. 2007; The ExpR/Sin quorum-sensing system controls succinoglycan production in Sinorhizobium meliloti . J Bacteriol 189:7077–7088
    [Google Scholar]
  18. Gonzalez J. E., Marketon M. M. 2003; Quorum sensing in nitrogen-fixing rhizobia. Microbiol Mol Biol Rev 67:574–592
    [Google Scholar]
  19. Hao G., Burr T. J. 2006; Regulation of long-chain N -acyl-homoserine lactones in Agrobacterium vitis . J Bacteriol 188:2173–2183
    [Google Scholar]
  20. Hao G., Zhang H., Zheng D., Burr T. J. 2005; luxR homolog avhR in Agrobacterium vitis affects the development of a grape-specific necrosis and a tobacco hypersensitive response. J Bacteriol 187:185–192
    [Google Scholar]
  21. Hoang H. H., Becker A., Gonzalez J. E. 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
    [Google Scholar]
  22. Hoang H. H., Gurich N., Gonzalez J. E. 2008; Regulation of motility by the ExpR/Sin quorum-sensing system in Sinorhizobium meliloti . J Bacteriol 190:861–871
    [Google Scholar]
  23. Janssens J. C., Metzger K., Daniels R., Ptacek D., Verhoeven T., Habel L. W., Vanderleyden J., De Vos D. E., De Keersmaecker S. C. 2007; Synthesis of N -acyl homoserine lactone analogues reveals strong activators of SdiA, the Salmonella enterica serovar Typhimurium LuxR homologue. Appl Environ Microbiol 73:535–544
    [Google Scholar]
  24. Kanamaru K., Kanamaru K., Tatsuno I., Tobe T., Sasakawa C. 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
    [Google Scholar]
  25. Lee J. H., Lequette Y., Greenberg E. P. 2006; Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59:602–609
    [Google Scholar]
  26. Lee J., Jayaraman A., Wood T. K. 2007; Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7:42
    [Google Scholar]
  27. Lequette Y., Lee J. H., Ledgham F., Lazdunski A., Greenberg E. P. 2006; A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188:3365–3370
    [Google Scholar]
  28. Lindsay A., Ahmer B. M. 2005; Effect of sdiA on biosensors of N -acylhomoserine lactones. J Bacteriol 187:5054–5058
    [Google Scholar]
  29. Marketon M. M., Glenn S. A., Eberhard A., Gonzalez J. E. 2003; Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti . J Bacteriol 185:325–331
    [Google Scholar]
  30. McIntosh M., Krol E., Becker A. 2008; Competitive and cooperative effects in quorum-sensing-regulated galactoglucan biosynthesis in Sinorhizobium meliloti . J Bacteriol 190:5308–5317
    [Google Scholar]
  31. Michael B., Smith J. N., Swift S., Heffron F., Ahmer B. M. 2001; SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 183:5733–5742
    [Google Scholar]
  32. Patankar A. V., Gonzalez J. E. 2009; An orphan LuxR homolog of Sinorhizobium meliloti affects stress adaptation and competition for nodulation. Appl Environ Microbiol 75:946–955
    [Google Scholar]
  33. Pellock B. J., Teplitski M., Boinay R. P., Bauer W. D., Walker G. C. 2002; A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti . J Bacteriol 184:5067–5076
    [Google Scholar]
  34. Rahmati S., Yang S., Davidson A. L., Zechiedrich E. L. 2002; Control of the AcrAB multidrug efflux pump by quorum sensing regulator SdiA. Mol Microbiol 43:677–685
    [Google Scholar]
  35. Rambow-Larsen A. A., Rajashekara G., Petersen E., Splitter G. 2008; Putative quorum-sensing regulator BlxR of Brucella melitensis regulates virulence factors including the type IV secretion system and flagella. J Bacteriol 190:3274–3282
    [Google Scholar]
  36. 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 U S A 93:336–341
    [Google Scholar]
  37. Slater H., Crow M., Everson L., Salmond G. P. 2003; Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol 47:303–320
    [Google Scholar]
  38. Smith J. N., Ahmer B. M. 2003; Detection of other microbial species by Salmonella : expression of the SdiA regulon. J Bacteriol 185:1357–1366
    [Google Scholar]
  39. Smith R. S., Iglewski B. H. 2003; P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6:56–60
    [Google Scholar]
  40. Smith J. N., Dyszel J. L., Soares J. A., Ellermeier C. D., Altier C., Lawhon S. D., Adams L. G., Konjufca V., Curtiss R. 3rd & other authors; 2008; SdiA, an N -acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS One 3:e2826
    [Google Scholar]
  41. Steindler L., Venturi V. 2007; Detection of quorum-sensing N -acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol Lett 266:1–9
    [Google Scholar]
  42. Taminiau B., Daykin M., Swift S., Boschiroli M. L., Tibor A., Lestrate P., De Bolle X., O'Callaghan D., Williams P., Letesson J. J. 2002; Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis . Infect Immun 70:3004–3011
    [Google Scholar]
  43. Uzureau S., Godefroid M., Deschamps C., Lemaire J., De Bolle X., Letesson J. J. 2007; Mutations of the quorum sensing-dependent regulator VjbR lead to drastic surface modifications in Brucella melitensis . J Bacteriol 189:6035–6047
    [Google Scholar]
  44. Walters M., Sperandio V. 2006; Quorum sensing in Escherichia coli and Salmonella . Int J Med Microbiol 296:125–131
    [Google Scholar]
  45. Waters C. M., Bassler B. L. 2005; Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346
    [Google Scholar]
  46. Whitehead N. A., Barnard A. M., Slater H., Simpson N. J., Salmond G. P. 2001; Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404
    [Google Scholar]
  47. Wilkinson A., Danino V., Wisniewski-Dye F., Lithgow J. K., Downie J. A. 2002; N -acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J Bacteriol 184:4510–4519
    [Google Scholar]
  48. Yao Y., Martinez-Yamout M. A., Dickerson T. J., Brogan A. P., Wright P. E., Dyson H. J. 2006; Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J Mol Biol 355:262–273
    [Google Scholar]
  49. Zhang L., Jia Y., Wang L., Fang R. 2007; A proline iminopeptidase gene upregulated in planta by a LuxR homologue is essential for pathogenicity of Xanthomonas campestris pv. campestris . Mol Microbiol 65:121–136
    [Google Scholar]
  50. Zheng D., Zhang H., Carle S., Hao G., Holden M. R., Burr T. J. 2003; A luxR homolog, aviR , in Agrobacterium vitis is associated with induction of necrosis on grape and a hypersensitive response on tobacco. Mol Plant Microbe Interact 16:650–658
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.026849-0
Loading
/content/journal/micro/10.1099/mic.0.026849-0
Loading

Data & Media loading...

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