1887

Microbiology Society logo

Volume 154, Issue 7

Regulation of autoinducer 2 production and expression in a pathogenic strain Free

Abstract

is a bacterial pathogen that can infect both humans and animals. TX1, an strain isolated from diseased fish, was found to produce autoinducer 2 (AI-2)-like activity that was growth phase dependent and modulated by growth conditions. The gene coding for the AI-2 synthase was cloned from TX1 and designated LuxS was able to complement the AI-2 mutant phenotype of strain DH5. Expression of correlated with AI-2 activity and was increased by glucose and decreased by elevated temperature. The effect of glucose was shown to be mediated through the cAMP-CRP complex, which repressed expression. Overexpression of enhanced AI-2 activity in TX1, whereas disruption of expression by antisense RNA interference (i) reduced the level of AI-2 activity, (ii) impaired bacterial growth under various conditions, (iii) weakened the expression of genes associated with the type III secretion system and biofilm formation, and (iv) attenuated bacterial virulence. Addition of exogenous AI-2 was able to complement the deficiencies in the expression of TTSS genes and biofilm production but failed to rescue the growth defects. Our results (i) demonstrated that the AI-2 activity in TX1 is controlled at least in part at the level of expression, which in turn is regulated by growth conditions, and that the temporal expression of is essential for optimal bacterial infection and survival; and (ii) suggested the existence in of a LuxS/AI-2-mediated signal transduction pathway that regulates the production of virulence-associated elements.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): AI-2, autoinducer 2 , CRP, cAMP receptor protein , EMSA, electrophoretic mobility shift assay , i.p., intraperitoneally , QS, quorum sensing , RITT, rho-independent transcriptional terminator and TTSS, type III secretion system
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/017343-0
2008-07-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/7/2060.html?itemId=/content/journal/micro/10.1099/mic.0.2008/017343-0&mimeType=html&fmt=ahah

References

  1. Bassler B. L., Wright M., Showalter R. E., Silverman M. R. 1993; Intercellular signaling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773–786
     [Google Scholar]
  2. Coulthurst S. J., Kurz C. L., Salmond G. P. C. 2004; luxS mutants of Serratia defective in autoinducer-2-dependent ‘quorum sensing’ show strain-dependent impacts on virulence and production of carbapenem and prodigiosin. Microbiology 150:1901–1910
     [Google Scholar]
  3. Coulthurst S. J., Clare S., Evans T. J., Foulds I. J., Roberts K. J., Welch M., Dougan G., Salmond G. P. C. 2007; Quorum sensing has an unexpected role in virulence in the model pathogen Citrobacter rodentium. EMBO Rep 8:698–703
     [Google Scholar]
  4. Day W. A., Maurelli A. T. 2001; Shigella flexneri LuxS quorum-sensing system modulates virB expression but is not essential for virulence. Infect Immun 69:15–23
     [Google Scholar]
  5. De Keersmaecker S. C. J., Sonck K., Vanderleyden J. 2006; Let LuxS speak up in AI-2 signaling. Trends Microbiol 14:114–119
     [Google Scholar]
  6. Doherty N., Holden M. T. G., Qazi S. N., Williams P., Winzer K. 2006; Functional analysis of luxS in Staphylococcus aureus reveals a role in metabolism but not quorum sensing. J Bacteriol 188:2885–2897
     [Google Scholar]
  7. Eagon R. G. 1962; Pseudomonas natriegens, a marine bacterium with a generation time of less than 10 minutes. J Bacteriol 83:736–737
     [Google Scholar]
  8. Gonzalez J. E., Keshavan N. D. 2006; Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70:859–875
     [Google Scholar]
  9. Gonzalez Barrios A. F., Zuo R., Hashimoto Y., Yang L., Bentley W. E., Wood T. K. 2006; Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022. J Bacteriol 188:305–316
     [Google Scholar]
  10. Henke J. M., Bassler B. L. 2004a; Bacterial social engagements. Trends Cell Biol 14:648–656
     [Google Scholar]
  11. Henke J. M., Bassler B. L. 2004b; Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186:3794–3805
     [Google Scholar]
  12. Herzberg M., Kaye I. K., Peti W., Wood T. K. 2006; YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J Bacteriol 188:587–598
     [Google Scholar]
  13. Hirono I., Tange N., Aoki T. 1997; Iron-regulated haemolysin gene from Edwardsiella tarda. Mol Microbiol 24:851–856
     [Google Scholar]
  14. Joyce E. A., Kawale A., Censini S., Kim C. C., Covacci A., Falkow S. 2004; LuxS is required for persistent pneumococcal carriage and expression of virulence and biosynthesis genes. Infect Immun 72:2964–2975
     [Google Scholar]
  15. Kendall M. M., Rasko D. A., Sperandio V. 2007; Global effects of the cell-to-cell signaling molecules autoinducer-2, autoinducer-3, and epinephrine in a luxS mutant of enterohemorrhagic Escherichia coli. Infect Immun 75:4875–4884
     [Google Scholar]
  16. Lewis H. A., Furlong E., Laubert B., Eroshkina G., Batiyenko Y., Adams J., Bergseid M., Marsh C., Peat T. other authors 2001; A structural genomics approach to the study of quorum sensing: crystal structures of three LuxS orthologs. Structure 9:527–537
     [Google Scholar]
  17. Li J., Attila C., Wang L., Wood T. K., Valdes J. J., Bentley W. E. 2007; Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 189:6011–6020
     [Google Scholar]
  18. Lyon W. R., Madden J. C., Levin J. C., Stein J. L., Caparon M. G. 2001; Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42:145–157
     [Google Scholar]
  19. Marouni M. J., Sela S. 2003; The luxS gene of Streptococcus pyogenes regulates expression of genes that affect internalization by epithelial cells. Infect Immun 71:5633–5639
     [Google Scholar]
  20. Marx C. J., Lidstrom M. E. 2001; Development of improved versatile broad-host range vectors for use in methylotrophs and other Gram-negative bacteria. Microbiology 147:2065–2075
     [Google Scholar]
  21. McNab R., Ford S. K., El-Sabaeny A., Barbieri B., Cook G. S., Lamont R. J. 2003; LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185:274–284
     [Google Scholar]
  22. Mok K. C., Wingreen N. S., Bassler B. L. 2003; Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 22:870–881
     [Google Scholar]
  23. Morohoshi T., Inaba T., Kato N., Kanai K., Ikeda T. 2004; Identification of quorum-sensing signal molecules and the LuxRI homologs in fish pathogen Edwardsiella tarda. J Biosci Bioeng 98:274–281
     [Google Scholar]
  24. Ohtani K., Hayashi H., Shimizu T. 2002; The luxS gene is involved in cell-cell signaling for toxin production in Clostridium perfringens. Mol Microbiol 44:171–179
     [Google Scholar]
  25. Rickard A. H., Palmer R. J., Blehert D. S., Campagna S. R., Semmelhack M. F., Egland P. G., Bassler B. L., Kolenbrander P. E. 2006; Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol 60:1446–1456
     [Google Scholar]
  26. Schauder S., Shokat K., Surette M. G., Bassler B. L. 2001; The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41:463–476
     [Google Scholar]
  27. Sircili M. P., Walters M., Trabulsi L. R., Sperandio V. 2004; Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect Immun 72:2329–2337
     [Google Scholar]
  28. Stroeher U. H., Paton A. W., Ogunniyi A. D., Paton J. C. 2003; Mutation of luxS of Streptococcus pneumoniae affects virulence in a mouse model. Infect Immun 71:3206–3212
     [Google Scholar]
  29. Sun L., vanderSpek J., Murphy J. R. 1998; Isolation and characterization of iron-independent positive dominant mutants of diphtheria toxin repressor, DtxR. Proc Natl Acad Sci U S A 95:14985–14990
     [Google Scholar]
  30. Sun L., Dove S. L., Panaghie G., deHaseth P., Hochschild A. 2004; An RNA polymerase mutant deficient in DNA melting facilitates study of activation mechanism: application to an artificial activator of transcription. J Mol Biol 343:1171–1182
     [Google Scholar]
  31. Surette M. G., Bassler B. L. 1998; Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci U S A 95:7046–7050
     [Google Scholar]
  32. Surette M. G., Bassler B. L. 1999; Regulation of autoinducer production in Salmonella typhimurium. Mol Microbiol 31:585–595
     [Google Scholar]
  33. 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 U S A 96:1639–1644
     [Google Scholar]
  34. Taga M. E., Semmelhack J. L., Bassler B. L. 2001; The LuxS-dependent autoinducer Al-2 controls the expression of an ABC transporter that functions in Al-2 uptake in Salmonella typhimurium. Mol Microbiol 42:777–793
     [Google Scholar]
  35. Taga M. E., Miller S. T., Bassler B. L. 2003; Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol Microbiol 50:1411–1427
     [Google Scholar]
  36. Tan Y. P., Zheng J., Tung S. L., Rosenshine I., Leung K. Y. 2005; Role of type III secretion in Edwardsiella tarda virulence. Microbiology 151:2301–2313
     [Google Scholar]
  37. Vendeville A., Winzer K., Heurlier K., Tang C. M., Hardie K. R. 2005; Making ‘sense’ of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Microbiol 3:383–396
     [Google Scholar]
  38. Wang L., Li J., March J. C., Valdes J. J., Bentley W. E. 2005; Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli. J Bacteriol 187:2066–2076
     [Google Scholar]
  39. Winzer K., Hardie K. R., Burgess N., Doherty N., Kirke D., Holden M. T. G., Linforth R., Cornell K. A., Taylor A. J. other authors 2002a; LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2 H)-furanone. Microbiology 148:909–922
     [Google Scholar]
  40. Winzer K., Sun Y. H., Green A., Delory M., Blackley D., Hardie K. R., Baldwin T. J., Tang C. M. 2002b; Role of Neisseria meningitidis luxS in cell-to-cell signaling and bacteremic infection. Infect Immun 70:2245–2248
     [Google Scholar]
  41. Xavier K. B., Bassler B. L. 2005; Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187:238–248
     [Google Scholar]
  42. Xu L., Li H., Vuong C., Vadyvaloo V., Wang J., Yao Y., Otto M., Gao Q. 2006; Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect Immun 74:488–496
     [Google Scholar]
  43. Zhang W. W., Sun L. 2007; Cloning, characterization and molecular application of a β-agarase gene from Vibrio sp. strain V134. Appl Environ Microbiol 73:2825–2831
     [Google Scholar]
  44. Zheng J., Leung K. 2007; Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66:1192–1206
     [Google Scholar]
  45. Zhu J., Miller M. B., Vance R. E., Dziejman M., Bassler B. L., Mekalanos J. J. 2002; Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 99:3129–3134
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/017343-0
Loading
Regulation of autoinducer 2 production and luxS expression in a pathogenic Edwardsiella tarda strain
Microbiology 154, 2060 (2008); https://doi.org/10.1099/mic.0.2008/017343-0
/content/journal/micro/10.1099/mic.0.2008/017343-0
/content/journal/micro/10.1099/mic.0.2008/017343-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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