1887

Abstract

The strain W2 has been shown previously to degrade the -acylhomoserine lactone (AHL) quorum-sensing signal molecule -hexanoyl--homoserine lactone, produced by other bacteria. Data presented here indicate that this Gram-positive bacterium is also capable of using various AHLs as the sole carbon and energy source. The enzymic activities responsible for AHL inactivation were investigated in cell extracts and in whole cells. cells rapidly degraded AHLs with 3-oxo substituents but exhibited relatively poor activity against the corresponding unsubstituted AHLs. Investigation of the mechanism(s) by which cells degraded AHLs revealed that 3-oxo compounds with -acyl side chains ranging from C to C were initially converted to their corresponding 3-hydroxy derivatives. This oxidoreductase activity was not specific to 3-oxo-AHLs but also allowed the reduction of compounds such as -(3-oxo-6-phenylhexanoyl)homoserine lactone (which contains an aromatic acyl chain substituent) and 3-oxododecanamide (which lacks the homoserine lactone ring). It also reduced both the - and -isomers of -(3-oxododecanoyl)--homoserine lactone. A second AHL-degrading activity was observed when cell extracts were incubated with -(3-oxodecanoyl)--homoserine lactone (3O,C10-HSL). This activity was both temperature- and pH-dependent and was characterized as an amidolytic activity by HPLC analysis of the reaction mixture treated with dansyl chloride. This revealed the accumulation of dansylated homoserine lactone, indicating that the 3O,C10-HSL amide had been cleaved to yield homoserine lactone. is therefore capable of modifying and degrading AHL signal molecules through both oxidoreductase and amidolytic activities.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27961-0
2005-10-01
2019-11-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/10/3313.html?itemId=/content/journal/micro/10.1099/mic.0.27961-0&mimeType=html&fmt=ahah

References

  1. Bock, C., Kroppenstedt, R. M. & Diekmann, H. ( 1996; ). Degradation and bioconversion of aliphatic and aromatic hydrocarbons by Rhodococcus ruber 219. Appl Microbiol Biotechnol 45, 408–410.[CrossRef]
    [Google Scholar]
  2. Byers, J. T., Lucas, C., Salmond, G. P. & Welch, M. ( 2002; ). Nonenzymatic turnover of an Erwinia carotovora quorum-sensing signalling molecule. J Bacteriol 184, 1163–1171.[CrossRef]
    [Google Scholar]
  3. Cámara, M., Williams, P. & Hardman, A. ( 2002; ). Controlling infection by tuning in and turning down the volume of bacterial small-talk. Lancet Infect Dis 2, 667–676.[CrossRef]
    [Google Scholar]
  4. Carlier, A., Uroz, S., Smadja, B., Fray, R., Latour, X., Dessaux, Y. & Faure, D. ( 2003; ). The Ti plasmid of Agrobacterium tumefaciens harbors an attM paralogous gene, aiiB, also encoding N-acylhomoserine lactonase activity. Appl Environ Microbiol 69, 4989–4993.[CrossRef]
    [Google Scholar]
  5. Carlier, A., Chevrot, R., Dessaux, Y. & Faure, D. ( 2004; ). In Agrobacterium tumefaciens strain C58, the assimilation of gamma-butyrolactone interferes with the accumulation of the N-acyl-homoserine lactone signal. Mol Plant Microbe Interact 17, 951–957.[CrossRef]
    [Google Scholar]
  6. Chauvaux, S., Chevalier, F., Le Dantec, C., Fayolle, F., Miras, I., Kunst, F. & Béguin, P. ( 2001; ). Cloning of a genetically unstable cytochrome P-450 gene cluster involved in degradation of the pollutant ethyl tert-butyl ether by Rhodococcus ruber. J Bacteriol 183, 6551–6557.[CrossRef]
    [Google Scholar]
  7. Chhabra, S. R., Stead, P., Bainton, N. J., Salmond, G. P. C., Stewart, G. S. A. B., Williams, P. & Bycroft, B. W. ( 1993; ). Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogues of N-(3-oxohexanoyl)-l-homoserine lactone. J Antibiot 46, 441–454.[CrossRef]
    [Google Scholar]
  8. Chhabra, S. R., Harty, C., Hooi, D. S. W., Daykin, M., Williams, P., Pritchard, D. I. & Bycroft, B. W. ( 2003; ). Synthetic analogues of bacterial quorum sensing molecules as immune modulators. J Med Chem 46, 97–104.[CrossRef]
    [Google Scholar]
  9. Chun, C. K., Ozer, E. A., Welsh, M. J., Zabner, J. & Greenberg, E. P. ( 2004; ). Inactivation of a Pseudomonas aeruginosa quorum-sensing signal by human airway epithelia. Proc Natl Acad Sci U S A 101, 3587–3590.[CrossRef]
    [Google Scholar]
  10. Delalande, L., Faure, F., Raffoux, A. & 8 other authors ( 2005; ). Plant-, temperature- and pH-dependent stability of hexanoyl-homoserine lactone, a mediator of quorum-sensing regulation. FEMS Microbiol Ecol 52, 13–20.[CrossRef]
    [Google Scholar]
  11. Dong, Y. H., Xu, J. L., Li, X. Z. & Zhang, L. H. ( 2000; ). AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci U S A 97, 3526–3531.[CrossRef]
    [Google Scholar]
  12. Dong, Y. H., Gusti, A. R., Zhang, Q., Xu, J. L. & Zhang, L. H. ( 2002; ). Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68, 1754–1759.[CrossRef]
    [Google Scholar]
  13. Fray, R. G. ( 2002; ). Altering plant-microbe interaction through artificially manipulating bacterial quorum sensing. Ann Bot 89, 245–253.[CrossRef]
    [Google Scholar]
  14. 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]
  15. Fuqua, C., Parsek, M. R. & Greenberg, E. P. ( 2001; ). Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35, 439–468.[CrossRef]
    [Google Scholar]
  16. Gardiner, S., Chhabra, S. R., Harty, C., Pritchard, D. I., Bycroft, B. W., Williams, P. & Bennett, T. ( 2001; ). Haemodynamic properties of bacterial quorum sensing signal molecules. Brit J Pharmacol 133, 1047–1054.[CrossRef]
    [Google Scholar]
  17. 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 signalling. J Bacteriol 178, 6618–6622.
    [Google Scholar]
  18. Haroune, N., Combourieu, B., Besse, P., Sancelme, M., Reemtsma, T., Kloepfer, A., Diab, A., Knapp, J. S., Baumberg, S. & Delort, A. M. ( 2002; ). Benzothiazole degradation by Rhodococcus pyridinovorans strain PA: evidence of a catechol 1,2-dioxygenase activity. Appl Environ Microbiol 68, 6114–6120.[CrossRef]
    [Google Scholar]
  19. Huang, J. J., Han, J., Zhang, L. & Leadbetter, J. R. ( 2003; ). Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 69, 5941–5949.[CrossRef]
    [Google Scholar]
  20. Jiang, Y., Camara, M., Chhabra, S. R., Hardie, K. R., Bycroft, B. W., Lazdunski, A., Salmond, G. P., Stewart, G. S. & Williams, P. ( 1998; ). In vitro biosynthesis of the Pseudomonas aeruginosa quorum sensing signal molecule N-butanoyl-l-homoserine lactone. Mol Microbiol 28, 193–203.
    [Google Scholar]
  21. Joint, I., Tait, K., Callow, M. E., Callow, J. A., Milton, D., Williams, P. & Camara, M. ( 2002; ). Cell-to-cell communication across the prokaryote/eukaryote boundary. Science 298, 1207.[CrossRef]
    [Google Scholar]
  22. 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 J 12, 2477–2482.
    [Google Scholar]
  23. Kang, B. R., Lee, J. H., Ko, S. J., Lee, Y. H., Cha, J. S., Cho, B. H. & Kim, Y. C. ( 2004; ). Degradation of acyl-homoserine lactone molecules by Acinetobacter sp. strain C1010. Can J Microbiol 50, 935–941.[CrossRef]
    [Google Scholar]
  24. Lamont, I. L. & Martin, L. W. ( 2003; ). Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology 149, 833–842.[CrossRef]
    [Google Scholar]
  25. Leadbetter, J. R. & Greenberg, E. P. ( 2000; ). Metabolism of acyl homoserine lactone quorum sensing signals by Variovorax paradoxus. J Bacteriol 182, 6921–6926.[CrossRef]
    [Google Scholar]
  26. Lee, S. J., Park, S. Y., Lee, J. J., Yum, D. Y., Koo, B. T. & Lee, J. K. ( 2002; ). Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl Environ Microbiol 68, 3919–3924.[CrossRef]
    [Google Scholar]
  27. Lin, Y. H., Xu, J. L., Hu, J., Wang, L. H., Ong, S. L., Leadbetter, J. R. & Zhang, L. H. ( 2003; ). Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 47, 849–860.[CrossRef]
    [Google Scholar]
  28. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anolles, G., Rolfe, B. G. & Bauer, W. D. ( 2003; ). Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci U S A 100, 1444–1449.[CrossRef]
    [Google Scholar]
  29. Milton, D. L., Hardman, A., Camara, M., Chhabra, S. R., Bycroft, B. W., Stewart, G. S. A. B. & Williams, P. ( 1997; ). Vibrio anguillarum produces multiple N-acylhomoserine lactone signal molecules. J Bacteriol 179, 3004–3012.
    [Google Scholar]
  30. Park, S. Y., Lee, S. J., Oh, T. K., Oh, J. W., Koo, B. T., Yum, D. Y. & Lee, J. K. ( 2003; ). AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149, 1541–1550.[CrossRef]
    [Google Scholar]
  31. Peters, L., König, G. M., Wright, A. D., Pukall, R., Stackebrandt, E., Eberl, L. & Riedel, K. ( 2003; ). Secondary metabolites of Flustra foliacea and their influence on bacteria. Appl Environ Microbiol 69, 3469–3475.[CrossRef]
    [Google Scholar]
  32. Reimmann, C., Ginet, N., Michel, L. & 9 other authors ( 2002; ). Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148, 923–932.
    [Google Scholar]
  33. Sakai, M., Miyauchi, K., Kato, N., Masai, E. & Fukuda, M. ( 2003; ). Cloning and heterologous expression of an enantioselective amidase from Rhodococcus erythropolis strain MP50. Appl Environ Microbiol 68, 3279–3286.
    [Google Scholar]
  34. Swift, S., Karlyshev, A. V., Durant, E. L., Winson, M. K., Williams, P., Macintyre, S. & Stewart, G. S. A. B. ( 1996; ). Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologues AhyRI and AsaRI and their cognate signal molecules. J Bacteriol 179, 5271–5281.
    [Google Scholar]
  35. Swift, S., Downie, J. A., Whitehead, N., Barnard, A. M. L., Salmond, G. P. C. & Williams, P. ( 2001; ). Quorum sensing as a population density dependent determinant of bacterial physiology. Adv Microb Physiol 45, 199–270.
    [Google Scholar]
  36. Telford, G., Wheeler, D., Williams, P., Tomkins, P. T., Appleby, P., Sewell, H., Stewart, G. S. A. B., Bycroft, B. W. & Pritchard, D. I. ( 1998; ). The Pseudomonas aeruginosa quorum sensing signal molecule, N-3-(oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun 66, 36–42.
    [Google Scholar]
  37. Teplistki, M., Robinson, J. B. & Bauer, W. D. ( 2000; ). Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviours in associated bacteria. Mol Plant Microbe Interact 13, 637–648.[CrossRef]
    [Google Scholar]
  38. Uroz, S., Dangelo, C., Carlier, A., Faure, D., Petit, A., Oger, P., Sicot, C. & Dessaux, Y. ( 2003; ). Novel bacteria degrading N-acyl homoserine lactones and their use as quenchers of quorum-sensing regulated functions of plant pathogenic bacteria. Microbiology 149, 1981–1989.[CrossRef]
    [Google Scholar]
  39. Van der Werf, M. J. & Boot, A. M. ( 2000; ). Metabolism of carveol and dihydrocarveol in Rhodococcus erythropolis DCL14. Microbiology 146, 1129–1141.
    [Google Scholar]
  40. Vaudequin-Dransart, V., Petit, A., Poncet, C., Ponsonnet, C., Nesme, X., Jones, J. B., Bouzar, H., Chilton, W. S. & Dessaux, Y. ( 1995; ). Novel Ti plasmids in Agrobacterium strains isolated from fig tree and chrysanthemum tumors and their opinelike molecules. Mol Plant Microbe Interact 8, 311–321.[CrossRef]
    [Google Scholar]
  41. Von Bodman, S. B., Bauer, W. D. & Coplin, D. L. ( 2003; ). Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41, 455–482.[CrossRef]
    [Google Scholar]
  42. Warhurst, A. M. & Fewson, C. A. ( 1994; ). Biotransformations catalyzed by the genus Rhodococcus. Crit Rev Biotechnol 14, 29–73.[CrossRef]
    [Google Scholar]
  43. Whitehead, N. A., Barnard, A. M. L., Slater, H., Simpson, N. J. L. & Salmond, G. P. C. ( 2001; ). Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25, 365–404.[CrossRef]
    [Google Scholar]
  44. Winans, S. C. & Bassler, B. L. ( 2002; ). Mob psychology. J Bacteriol 184, 873–883.[CrossRef]
    [Google Scholar]
  45. Winson, M. K., Swift, S., Fish, L., Throup, J. P., Jorgensen, F., Chhabra, S. R., Bycroft, B. W., Williams, P. & Stewart, G. S. A. B. ( 1998; ). Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acylhomoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163, 185–192.[CrossRef]
    [Google Scholar]
  46. Winzer, K., Hardie, K. & Williams, P. ( 2002; ). Bacterial cell-to-cell communication: sorry, can't talk now – gone to lunch! Curr Opin Microbiol 5, 216–222.[CrossRef]
    [Google Scholar]
  47. Yates, E. A., Philipp, B., Buckley, C. & 8 other authors ( 2002; ). N-acyl homoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70, 5635–5646.[CrossRef]
    [Google Scholar]
  48. Zelinski, T. & Kula, M. R. ( 1994; ). A kinetic study and application of a novel carbonyl reductase isolated from Rhodococcus erythroplis. Bioorg Med Chem 2, 421–428.[CrossRef]
    [Google Scholar]
  49. Zelinski, T., Peters, J. & Kula, M. R. ( 1994; ). Purification and characterization of a novel carbonyl reductase isolated from Rhodococcus erythropolis. J Biotechnol 33, 283–292.[CrossRef]
    [Google Scholar]
  50. Zhang, L., Murphy, P. J., Kerr, A. & Tate, M. E. ( 1993; ). Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones. Nature 362, 446–450.[CrossRef]
    [Google Scholar]
  51. Zhang, H. B., Wang, L. H. & Zhang, L. H. ( 2002; ). Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 99, 4638–4643.[CrossRef]
    [Google Scholar]
  52. Zhu, J. & Winans, S. C. ( 2001; ). The quorum-sensing transcriptional regulator TraR requires its cognate signalling ligand for protein folding, protease resistance and dimerisation. Proc Natl Acad Sci U S A 98, 1507–1512.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27961-0
Loading
/content/journal/micro/10.1099/mic.0.27961-0
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