1887

Abstract

is the causative agent of human and animal melioidosis. The role of quorum sensing (QS) in the pathogenicity of via inhalational exposure of BALB/c mice and intraperitoneal challenge of Syrian hamsters has not been reported. This investigation demonstrates that encodes a minimum of three and five homologues that are involved in animal pathogenicity. Mass spectrometry analysis of culture supernatants revealed that wild-type and the mutants synthesized numerous signalling molecules, including -octanoyl-homoserine lactone, -decanoyl-homoserine lactone, -(3-hydroxyoctanoyl)--homoserine lactone, -(3-hydroxydecanoyl)--homoserine lactone and -(3-oxotetradecanoyl)--homoserine lactone, which was further confirmed by heterologous expression of the alleles in . Mutagenesis of the QS system increased the time to death and reduced organ colonization of aerosolized BALB/c mice. Further, intraperitoneal challenge of Syrian hamsters with the QS mutants resulted in a significant increase in the LD Using semi-quantitative plate assays, preliminary analysis suggests that QS does not affect lipase, protease and phospholipase C biosynthesis/secretion in . The findings of the investigation demonstrate that encodes multiple genes, and disruption of the QS alleles reduces animal pathogenicity, but does not affect exoproduct secretion.

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2004-11-01
2019-11-20
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References

  1. Aguilar, C., Bertani, I. & Venturi, V. ( 2003;). Quorum-sensing system and stationary-phase sigma factor (rpoS) of the onion pathogen Burkholderia cepacia genomovar I type strain, ATCC 25416. Appl Environ Microbiol 69, 1739–1747.[CrossRef]
    [Google Scholar]
  2. Baldwin, A., Sokol, P. A., Parkhill, J. & Mahenthiralingam, E. ( 2004;). The Burkholderia cepacia epidemic strain marker is part of a novel genomic island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia. Infect Immun 72, 1537–1547.[CrossRef]
    [Google Scholar]
  3. Brint, J. M. & Ohman, D. E. ( 1995;). Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol 177, 7155–7163.
    [Google Scholar]
  4. Chapon-Herve, V., Akrim, M., Latifi, A., Williams, P., Lazdunski, A. & Bally, M. ( 1997;). Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol Microbiol 24, 1169–1178.[CrossRef]
    [Google Scholar]
  5. Conway, B. A. & Greenberg, E. P. ( 2002;). Quorum-sensing signals and quorum-sensing genes in Burkholderia vietnamiensis. J Bacteriol 184, 1187–1191.[CrossRef]
    [Google Scholar]
  6. Dance, D. A. ( 2002;). Melioidosis. Curr Opin Infect Dis 15, 127–132.[CrossRef]
    [Google Scholar]
  7. DeShazer, D. & Waag, D. M. ( 2004;). Glanders: new insights into an old disease. In Biological Weapons Defense: Infectious Diseases and Counterbioterrorism. Edited by L. Lindler, F. Lebeda & G. W. Korch. Totowa, NJ: Humana Press (in press).
  8. DeShazer, D., Brett, P. J., Carlyon, R. & Woods, D. E. ( 1997;). Mutagenesis of Burkholderia pseudomallei with Tn5-OT182: isolation of motility mutants and molecular characterization of the flagellin structural gene. J Bacteriol 179, 2116–2125.
    [Google Scholar]
  9. DeShazer, D., Brett, P. J. & Woods, D. E. ( 1998;). The type II O-antigenic polysaccharide moiety of Burkholderia pseudomallei lipopolysaccharide is required for serum resistance and virulence. Mol Microbiol 30, 1081–1100.[CrossRef]
    [Google Scholar]
  10. DeShazer, D., Brett, P. J., Burtnick, M. N. & Woods, D. E. ( 1999;). Molecular characterization of genetic loci required for secretion of exoproducts in Burkholderia pseudomallei. J Bacteriol 181, 4661–4664.
    [Google Scholar]
  11. DeShazer, D., Waag, D. M., Fritz, D. L. & Woods, D. E. ( 2001;). Identification of a Burkholderia mallei polysaccharide gene cluster by subtractive hybridization and demonstration that the encoded capsule is an essential virulence determinant. Microb Pathog 30, 253–269.[CrossRef]
    [Google Scholar]
  12. Donabedian, H. ( 2003;). Quorum sensing and its relevance to infectious diseases. J Infect 46, 207–214.[CrossRef]
    [Google Scholar]
  13. Fuqua, C. & Winans, S. C. ( 1996;). Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J Bacteriol 178, 435–440.
    [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. Gambello, M. J., Kaye, S. & Iglewski, B. H. ( 1993;). LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infect Immun 61, 1180–1184.
    [Google Scholar]
  17. Godoy, D., Randle, G., Simpson, A. J., Aanensen, D. M., Pitt, T. L., Kinoshita, R. & Spratt, B. G. ( 2003;). Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei. J Clin Microbiol 41, 2068–2079.[CrossRef]
    [Google Scholar]
  18. Gotschlich, A., Huber, B., Geisenberger, O. & 11 other authors ( 2001;). Synthesis of multiple N-acylhomoserine lactones is wide-spread among the members of the Burkholderia cepacia complex. Syst Appl Microbiol 24, 1–14.[CrossRef]
    [Google Scholar]
  19. Hardman, A. M., Stewart, G. S. & Williams, P. ( 1998;). Quorum sensing and the cell-cell communication dependent regulation of gene expression in pathogenic and non-pathogenic bacteria. Antonie van Leeuwenhoek 74, 199–210.[CrossRef]
    [Google Scholar]
  20. Latifi, A., Winson, M. K., Foglino, M., Bycroft, B. W., Stewart, G. S., Lazdunski, A. & Williams, P. ( 1995;). Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol 17, 333–343.[CrossRef]
    [Google Scholar]
  21. 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 RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21, 1137–1146.[CrossRef]
    [Google Scholar]
  22. Lewenza, S. & Sokol, P. A. ( 2001;). Regulation of ornibactin biosynthesis and N-acyl-l-homoserine lactone production by CepR in Burkholderia cepacia. J Bacteriol 183, 2212–2218.[CrossRef]
    [Google Scholar]
  23. Lewenza, S., Conway, B., Greenberg, E. P. & Sokol, P. A. ( 1999;). Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 181, 748–756.
    [Google Scholar]
  24. McKenney, D., Brown, K. E. & Allison, D. G. ( 1995;). Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication. J Bacteriol 177, 6989–6992.
    [Google Scholar]
  25. Moore, R. A., DeShazer, D., Reckseidler, S., Weissman, A. & Woods, D. E. ( 1999;). Efflux-mediated aminoglycoside and macrolide resistance in Burkholderia pseudomallei. Antimicrob Agents Chemother 43, 465–470.
    [Google Scholar]
  26. Ochsner, U. A. & Reiser, J. ( 1995;). Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92, 6424–6428.[CrossRef]
    [Google Scholar]
  27. Ochsner, U. A., Koch, A. K., Fiechter, A. & Reiser, J. ( 1994;). Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol 176, 2044–2054.
    [Google Scholar]
  28. Parsek, M. R., Schaefer, A. L. & Greenberg, E. P. ( 1997;). Analysis of random and site-directed mutations in rhII, a Pseudomonas aeruginosa gene encoding an acylhomoserine lactone synthase. Mol Microbiol 26, 301–310.[CrossRef]
    [Google Scholar]
  29. Passador, L., Cook, J. M., Gambello, M. J., Rust, L. & Iglewski, B. H. ( 1993;). Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260, 1127–1130.[CrossRef]
    [Google Scholar]
  30. Pearson, J. P., Pesci, E. C. & Iglewski, B. H. ( 1997;). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179, 5756–5767.
    [Google Scholar]
  31. Pearson, J. P., Feldman, M., Iglewski, B. H. & Prince, A. ( 2000;). Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect Immun 68, 4331–4334.[CrossRef]
    [Google Scholar]
  32. Reckseidler, S. L., DeShazer, D., Sokol, P. A. & Woods, D. E. ( 2001;). Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect Immun 69, 34–44.[CrossRef]
    [Google Scholar]
  33. Roy, C. J., Hale, M., Hartings, J. M., Pitt, L. & Duniho, S. ( 2003;). Impact of inhalation exposure modality and particle size on the respiratory deposition of ricin in BALB/c mice. Inhal Toxicol 15, 619–638.[CrossRef]
    [Google Scholar]
  34. Rumbaugh, K. P., Griswold, J. A., Iglewski, B. H. & Hamood, A. N. ( 1999;). Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect Immun 67, 5854–5862.
    [Google Scholar]
  35. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989;). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  36. Schuster, M., Lostroh, C. P., Ogi, T. & Greenberg, E. P. ( 2003;). Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185, 2066–2079.[CrossRef]
    [Google Scholar]
  37. Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E., Jr, Rinehart, K. L. & Farrand, S. K. ( 1997;). Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci U S A 94, 6036–6041.[CrossRef]
    [Google Scholar]
  38. Simon, R., Priefer, U. & Pühler, A. ( 1983;). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology 1, 784–791.[CrossRef]
    [Google Scholar]
  39. Sokol, P. A., Sajjan, U., Visser, M. B., Gingues, S., Forstner, J. & Kooi, C. ( 2003;). The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149, 3649–3658.[CrossRef]
    [Google Scholar]
  40. Stevens, M. P., Wood, M. W., Taylor, L. A., Monaghan, P., Hawes, P., Jones, P. W., Wallis, T. S. & Galyov, E. E. ( 2002;). An Inv/Mxi-Spa-like type III protein secretion system in Burkholderia pseudomallei modulates intracellular behaviour of the pathogen. Mol Microbiol 46, 649–659.[CrossRef]
    [Google Scholar]
  41. Ulett, G. C., Currie, B. J., Clair, T. W. & 9 other authors ( 2001;). Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect 3, 621–631.[CrossRef]
    [Google Scholar]
  42. Ulrich, R. L. & DeShazer, D. ( 2004;). Type III secretion: a virulence factor delivery system essential for the pathogenicity of Burkholderia mallei. Infect Immun 72, 1150–1154.[CrossRef]
    [Google Scholar]
  43. Ulrich, R. L., Hines, H. B., Parthasarathy, N. & Jeddeloh, J. A. ( 2004;). Mutational analysis and biochemical characterization of the Burkholderia thailandensis DW503 quorum-sensing network. J Bacteriol 186, 4350–4360.[CrossRef]
    [Google Scholar]
  44. Valade, E., Thibault, F. M., Gauthier, Y. P., Palencia, M., Popoff, M. Y. & Vidal, D. R. ( 2004;). The PmlI-PmlR quorum-sensing system in Burkholderia pseudomallei plays a key role in virulence and modulates production of the MprA protease. J Bacteriol 186, 2288–2294.[CrossRef]
    [Google Scholar]
  45. Wagner, V. E., Bushnell, D., Passador, L., Brooks, A. I. & Iglewski, B. H. ( 2003;). Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185, 2080–2095.[CrossRef]
    [Google Scholar]
  46. Woods, D. E., DeShazer, D., Moore, R. A., Brett, P. J., Burtnick, M. N., Reckseidler, S. L. & Senkiw, M. D. ( 1999;). Current studies on the pathogenesis of melioidosis. Microbes Infect 1, 157–162.[CrossRef]
    [Google Scholar]
  47. Wu, H., Song, Z., Givskov, M., Doring, G., Worlitzsch, D., Mathee, K., Rygaard, J. & Hoiby, N. ( 2001;). Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology 147, 1105–1113.
    [Google Scholar]
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