1887

Abstract

-acyl-L-homoserine lactones (AHLs) are co-regulatory ligands required for control of the expression of genes encoding virulence traits in many Gram-negative bacterial species. Recent studies have indicated that AHLs modulate the cellular concentrations of LuxR-type regulatory proteins by binding and fortifying these proteins against proteolytic degradation (Zhu & Winans, 2001 ). Halogenated furanones produced by the macroalga inhibit AHL-dependent gene expression. This study assayed for an interaction between a tritiated halogenated furanone and the LuxR protein of overproduced in . Whilst a stable interaction between the algal metabolite and the bacterial protein was not found, it was noted by Western analysis that the half-life of the protein is reduced up to 100-fold in the presence of halogenated furanones. This suggests that halogenated furanones modulate LuxR activity but act to destabilize, rather than protect, the AHL-dependent transcriptional activator. The furanone-dependent reduction in the cellular concentration of the LuxR protein was associated with a reduction in expression of a plasmid encoded (ASV) fusion suggesting that the reduction in LuxR concentration is the mechanism by which furanones control expression of AHL-dependent phenotypes. The mode of action by which halogenated furanones reduce cellular concentrations of the LuxR protein remains to be characterized.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-4-1119
2002-04-01
2020-02-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/4/1481119a.html?itemId=/content/journal/micro/10.1099/00221287-148-4-1119&mimeType=html&fmt=ahah

References

  1. Adar Y. Y., Simaan M., Ulitzur S. 1992; Formation of the LuxR protein in the Vibrio fischeri lux system is controlled by HtpR through the GroESL proteins. J Bacteriol174:7138–7143
    [Google Scholar]
  2. Albus A. M., Pesci E. C., Runyen-Janecky L. J., West S. E., Iglewski B. H. 1997; Vfr controls quorum sensing in Pseudomonas aeruginosa . J Bacteriol179:3928–3935
    [Google Scholar]
  3. Andersen J. B., Sternberg C., Poulsen L. K., Bjørn S. P., Givskov M., Molin S. 1998; New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol64:2240–2246
    [Google Scholar]
  4. Andersen J. B., Heydorn A., Hentzer M., Eberl L., Geisenberger O., Molin S., Givskov M. 2001; gfp based N -acyl-homoserine-lactone monitors for detection of bacterial communication. Appl Environ Microbiol67:575–585[CrossRef]
    [Google Scholar]
  5. Bainton N. J., Bycroft B. W., Chhabra S. R.. 8 other authors 1992; A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia . Gene116:87–91[CrossRef]
    [Google Scholar]
  6. Barras F., van Gijsegem F., Chatterjee A. K. 1994; Extracellular enzymes and pathogenesis of soft rot Erwinia . Annu Rev Phytopathol32:201–234[CrossRef]
    [Google Scholar]
  7. 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 Microbiol9:773–786[CrossRef]
    [Google Scholar]
  8. Choi S. H., Greenberg E. P. 1992; Genetic evidence for the multimerization of LuxR, the transcriptional activator of Vibrio fischeri luminescence. Mol Mar Biol Biotechnol1:408–413
    [Google Scholar]
  9. Clark D. J., Maaløe O. 1967; DNA replication and division cycle in Escherichia coli . J Mol Biol23:99–112[CrossRef]
    [Google Scholar]
  10. Correa J. A. 1996; Diseases in seaweeds: an introduction. Hydrobiologia326:87–88
    [Google Scholar]
  11. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science280:295–298[CrossRef]
    [Google Scholar]
  12. de Nys R., Wright A. D., Konig G. M., Sticher O. 1993; New halogenated furanones from the marine alga Delisea pulchra (cf. Fimbriata). Tetrahedron49:11213–11220[CrossRef]
    [Google Scholar]
  13. Dworjanyn S. A., de Nys R., Steinberg P. D. 1999; Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra . Mar Biol133:727–736[CrossRef]
    [Google Scholar]
  14. Eberhard A., Burlingame A. L., Eberhard C., Kenyon G. L., Nealson K. H., Oppenheimer N. J. 1981; Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry20:2444–2449[CrossRef]
    [Google Scholar]
  15. Eberl L. 1999; N -Acyl homoserine lactone-mediated gene regulation in Gram-negative bacteria. Syst Appl Microbiol22:493–506[CrossRef]
    [Google Scholar]
  16. Eberl L., Molin S., Givskov M. 1999; Surface motility in Serratia liquefaciens . J Bacteriol181:1703–1712
    [Google Scholar]
  17. Fenical W. 1997; New pharmaceuticals from marine organisms. Trends Biotechnol15:339–341[CrossRef]
    [Google Scholar]
  18. 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]
  19. Fuqua C., Winans S. C., Greenberg E. P. 1996; Census and consensus in bacterial ecosystems: the LuxR–LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol50:727–751[CrossRef]
    [Google Scholar]
  20. Givskov M., de Nys R., Manefield M., Gram L., Maximilien R., Eberl L., Molin S., Steinberg P. D., Kjelleberg S. 1996; Eukaryotic interference with homoserine lactone mediated prokaryotic signaling. J Bacteriol178:6618–6622
    [Google Scholar]
  21. Goloubinoff P., Gatenby A. A., Lorimer G. H. 1989; GroE heat-shock proteins promote the assembly of foreign prokaryotic ribulose biphosphate carboxylase oligomers in Escherichia coli . Nature337:44–47[CrossRef]
    [Google Scholar]
  22. Guyer M. S., Reed R. E., Steitz T., Low K. B. 1981; Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harbor Symp Quant Biol45:135–140[CrossRef]
    [Google Scholar]
  23. Hanzelka B. L., Greenberg E. P. 1995; Evidence that the N -terminal region of the Vibrio fischeri LuxR protein constitutes an autoinducer-binding domain. J Bacteriol177:815–817
    [Google Scholar]
  24. Jones S., Yu B., Bainton N. J.. 11 other authors 1993; The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa . EMBO J12:2477–2482
    [Google Scholar]
  25. Kievit T. R., Iglewski B. 2000; Bacterial quorum sensing in pathogenic relationships. Infect Immun68:4839–4849[CrossRef]
    [Google Scholar]
  26. Kjelleberg S., Steinberg P. 2001; Defences against bacterial colonisation of marine plants. In Phyllosphere Microbiology pp157–172 Edited by Lindow S. E., Hecht-Poinar E., Elliot V.. St Paul, MN: American Phytopathological Society;
    [Google Scholar]
  27. Kjelleberg S., Steinberg P., Givskov M., Gram L., Manefield M., de Nys R. 1997; Do marine natural products interfere with prokaryotic AHL regulatory systems?. Aquat Microbial Ecol13:85–93[CrossRef]
    [Google Scholar]
  28. Manefield M., de Nys R., Kumar N., Read R., Givskov M., Steinberg P., Kjelleberg S. 1999; Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology145:283–291[CrossRef]
    [Google Scholar]
  29. Manny A. J., Kjelleberg S., Kumar N., de Nys R., Read R. W., Steinberg P. 1997; Reinvestigation of the sulfuric acid-catalysed cyclisation of brominated 2-alkyllevulinic acids to 3-alkyl-5-methylene-2(5 H )-furanones. Tetrahedron 53:15813–15826[CrossRef]
    [Google Scholar]
  30. McClean K. H., Winson M. K., Fish L.. 9 other authors 1997; Quorum sensing and Chromobacterium violaceum : exploitation of violacein production and inhibition for the detection of N -acylhomoserine lactones. Microbiology143:3703–3711[CrossRef]
    [Google Scholar]
  31. Nealson K. H., Eberhard A., Hastings J. W. 1972; Catabolite repression of bacterial bioluminescence: functional implications. Proc Natl Acad Sci USA69:1073–1076[CrossRef]
    [Google Scholar]
  32. Piper K., Beck von Bodman S., Farrand S. K. 1993; Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature362:448–450[CrossRef]
    [Google Scholar]
  33. Qin Y., Luo Z., Smyth A. J., Gao P., Beck von Bodman S., Farrand S. K. 2000; Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm. EMBO J19:5212–5221[CrossRef]
    [Google Scholar]
  34. Rasmussen T. B., Manefield M., Andersen J. B., Eberl L., Anthoni U., Christophersen C., Steinberg P., Kjelleberg S., Givskov M. 2000; How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology146:3237–3244
    [Google Scholar]
  35. 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]
  36. Sitnikov D. M., Schineller J. B., Baldwin T. O. 1995; Transcriptional regulation of bioluminesence genes from Vibrio fischeri . Mol Microbiol17:801–812[CrossRef]
    [Google Scholar]
  37. Swift S., Williams P., Stewart G. S. A. B. 1999; N -Acylhomoserine 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]
  38. Ulitzur S., Matin A., Fraley C., Meighen E. 1997; H-NS protein represses transcription of the lux systems of Vibrio fischeri and other luminous bacteria cloned into Escherichia coli . Curr Microbiol35:336–342[CrossRef]
    [Google Scholar]
  39. Welch M., Todd D. E., Whitehead N. A., McGowan S. J., Bycroft B. A., Salmond G. P. C. 2000; N -acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia . EMBO J19:631–641[CrossRef]
    [Google Scholar]
  40. Wells P. R. 1963; Enol lactones of dibromoacetylacrylic acid. Aust J Chem16:165–169[CrossRef]
    [Google Scholar]
  41. Zhang L., Murphy P. J., Kerr A., Tate M. E. 1993; Agrobacterium conjugation and gene regulation by N -acyl-l-homoserine lactones. Nature362:446–448[CrossRef]
    [Google Scholar]
  42. Zhu J., Winans S. C. 1999; Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. Proc Natl Acad Sci USA96:4832–4837[CrossRef]
    [Google Scholar]
  43. Zhu J., Winans S. C. 2001; The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc Natl Acad Sci USA98:1507–1512[CrossRef]
    [Google Scholar]
  44. Zhu J., Beaber J. W., More M. I., Fuqua C., Eberhard A., Winans S. C. 1998; Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens . J Bacteriol180:5398–5405
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-4-1119
Loading
/content/journal/micro/10.1099/00221287-148-4-1119
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