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
2024-11-05
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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 Lindler L., Lebeda F., Korch G. W. Totowa, NJ: Humana Press; (in press
    [Google Scholar]
  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;
    [Google Scholar]
  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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