1887

Microbiology Society logo

Volume 158, Issue 1

The two-component QseBC signalling system regulates and virulence of Free

Abstract

We recently demonstrated that the -acylhomoserine lactone [autoinducer (AI)-1] and LuxS (AI-2)-based quorum-sensing (QS) systems exerted positive and negative regulation, respectively, on the virulence of a diarrhoeal isolate SSU of . However, the role of a newly identified, two-component-based QseBC QS system in the regulation of bacterial virulence in general is not well understood, with only a limited number of studies showing its function in bacterial pathogenesis. In this report, we identified and characterized the QseBC QS system in SSU and found that, as was the case with enterohaemorrhagic , the open reading frames for the (the response regulator) and (the sensor histidine kinase) genes overlapped by 4 bp at the ATGA motif. Our data provide evidence that deletion of the gene from resulted in attenuation of bacterial virulence in a septicaemic mouse model of infection and diminished swimming and swarming motility, and the mutant bacteria formed denser biofilms compared with those from the parental strain of . The decrease in the virulence of the Δ mutant correlated with reduced production of protease and the cytotoxic enterotoxin, which has associated haemolytic activity. The swimming and swarming motility, haemolytic activity, protease production and biofilm formation were restored in the complemented strain to a level similar to that of the wild-type . SSU. Our study is the first, to our knowledge, to report a functional QseBC QS system in . which may be linked to AI-1 and AI-2 QS systems in modulating bacterial virulence, possibly through the cyclic diguanosine monophosphate.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© 2012 SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.051805-0
2012-01-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/1/259.html?itemId=/content/journal/micro/10.1099/mic.0.051805-0&mimeType=html&fmt=ahah

References

  1. Abuhammour W., Hasan R. A., Rogers D. ( 2006). Necrotizing fasciitis caused by Aeromonas hydrophilia in an immunocompetent child. Pediatr Emerg Care 22:48–51 [View Article][PubMed]
     [Google Scholar]
  2. Albert M. J., Ansaruzzaman M., Talukder K. A., Chopra A. K., Kuhn I., Rahman M., Faruque A. S., Islam M. S., Sack R. B., Mollby R. ( 2000). Prevalence of enterotoxin genes in Aeromonas spp. isolated from children with diarrhea, healthy controls, and the environment. J Clin Microbiol 38:3785–3790[PubMed]
     [Google Scholar]
  3. Bearson B. L., Bearson S. M. ( 2008). The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microb Pathog 44:271–278 [View Article][PubMed]
     [Google Scholar]
  4. Bearson B. L., Bearson S. M., Lee I. S., Brunelle B. W. ( 2010). The Salmonella enterica serovar Typhimurium QseB response regulator negatively regulates bacterial motility and swine colonization in the absence of the QseC sensor kinase. Microb Pathog 48:214–219 [View Article][PubMed]
     [Google Scholar]
  5. Beier D., Gross R. ( 2006). Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9:143–152 [View Article][PubMed]
     [Google Scholar]
  6. Challapalli M., Tess B. R., Cunningham D. G., Chopra A. K., Houston C. W. ( 1988). Aeromonas-associated diarrhea in children. Pediatr Infect Dis J 7:693–698 [View Article][PubMed]
     [Google Scholar]
  7. Chopra A. K., Houston C. W. ( 1999). Enterotoxins in Aeromonas-associated gastroenteritis. Microbes Infect 1:1129–1137 [View Article][PubMed]
     [Google Scholar]
  8. Chopra A. K., Xu X., Ribardo D., Gonzalez M., Kuhl K., Peterson J. W., Houston C. W. ( 2000). The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infect Immun 68:2808–2818 [View Article][PubMed]
     [Google Scholar]
  9. Clarke M. B., Sperandio V. ( 2005a). Transcriptional regulation of flhDC by QseBC and sigma (FliA) in enterohaemorrhagic Escherichia coli . Mol Microbiol 57:1734–1749 [View Article][PubMed]
     [Google Scholar]
  10. Clarke M. B., Sperandio V. ( 2005b). Transcriptional autoregulation by quorum sensing Escherichia coli regulators B and C (QseBC) in enterohaemorrhagic E. coli (EHEC). Mol Microbiol 58:441–455 [View Article][PubMed]
     [Google Scholar]
  11. Clarke M. B., Hughes D. T., Zhu C., Boedeker E. C., Sperandio V. ( 2006). The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci U S A 103:10420–10425 [View Article][PubMed]
     [Google Scholar]
  12. Costerton J. W., Cheng K. J., Geesey G. G., Ladd T. I., Nickel J. C., Dasgupta M., Marrie T. J. ( 1987). Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464 [View Article][PubMed]
     [Google Scholar]
  13. Costerton J. W., Stewart P. S., Greenberg E. P. ( 1999). Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322 [View Article][PubMed]
     [Google Scholar]
  14. de Kievit T. R. ( 2009). Quorum sensing in Pseudomonas aeruginosa biofilms. Environ Microbiol 11:279–288 [View Article][PubMed]
     [Google Scholar]
  15. Edwards R. A., Keller L. H., Schifferli D. M. ( 1998). Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207:149–157 [View Article][PubMed]
     [Google Scholar]
  16. Erova T. E., Pillai L., Fadl A. A., Sha J., Wang S., Galindo C. L., Chopra A. K. ( 2006). DNA adenine methyltransferase influences the virulence of Aeromonas hydrophila . Infect Immun 74:410–424 [View Article][PubMed]
     [Google Scholar]
  17. Erova T. E., Sha J., Horneman A. J., Borchardt M. A., Khajanchi B. K., Fadl A. A., Chopra A. K. ( 2007). Identification of a new hemolysin from diarrheal isolate SSU of Aeromonas hydrophila . FEMS Microbiol Lett 275:301–311 [View Article][PubMed]
     [Google Scholar]
  18. Figueras M. J., Aldea M. J., Fernández N., Aspíroz C., Alperi A., Guarro J. ( 2007). Aeromonas hemolytic uremic syndrome. A case and a review of the literature. Diagn Microbiol Infect Dis 58:231–234 [View Article][PubMed]
     [Google Scholar]
  19. Galindo C. L., Fadl A. A., Sha J., Gutierrez C. Jr, Popov V. L., Boldogh I., Aggarwal B. B., Chopra A. K. ( 2004). Aeromonas hydrophila cytotoxic enterotoxin activates mitogen-activated protein kinases and induces apoptosis in murine macrophages and human intestinal epithelial cells. J Biol Chem 279:37597–37612 [View Article][PubMed]
     [Google Scholar]
  20. Galindo C. L., Gutierrez C. Jr, Chopra A. K. ( 2006). Potential involvement of galectin-3 and SNAP23 in Aeromonas hydrophila cytotoxic enterotoxin-induced host cell apoptosis. Microb Pathog 40:56–68 [View Article][PubMed]
     [Google Scholar]
  21. Hengge R. ( 2009). Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273 [View Article][PubMed]
     [Google Scholar]
  22. Hiransuthikul N., Tantisiriwat W., Lertutsahakul K., Vibhagool A., Boonma P. ( 2005). Skin and soft-tissue infections among tsunami survivors in southern Thailand. Clin Infect Dis 41:e93–e96 [View Article][PubMed]
     [Google Scholar]
  23. Hoch J. A. ( 2000). Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3:165–170 [View Article][PubMed]
     [Google Scholar]
  24. Horneman A. J., Ali A., Abbott S. ( 2007). Aeromonas. Manual of Clinical Microbiology, 9th edn. Murray P. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  25. Hughes D. T., Clarke M. B., Yamamoto K., Rasko D. A., Sperandio V. ( 2009). The QseC adrenergic signaling cascade in enterohemorrhagic E. coli (EHEC). PLoS Pathog 5:e1000553 [View Article][PubMed]
     [Google Scholar]
  26. Huq A., Whitehouse C. A., Grim C. J., Alam M., Colwell R. R. ( 2008). Biofilms in water, its role and impact in human disease transmission. Curr Opin Biotechnol 19:244–247 [View Article][PubMed]
     [Google Scholar]
  27. Janda J. M. ( 1991). Recent advances in the study of the taxonomy, pathogenicity, and infectious syndromes associated with the genus Aeromonas . Clin Microbiol Rev 4:397–410[PubMed]
     [Google Scholar]
  28. Janda J. M. ( 2002). Aeromonas and Plesiomonas. Molecular Medical Microbiology vol. 21237–1270 Sussman M. London, UK: Academic Press; [View Article]
     [Google Scholar]
  29. Janda J. M., Abbott S. L. ( 2010). The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23:35–73 [View Article][PubMed]
     [Google Scholar]
  30. Kaper J. B., Sperandio V. ( 2005). Bacterial cell-to-cell signaling in the gastrointestinal tract. Infect Immun 73:3197–3209 [View Article][PubMed]
     [Google Scholar]
  31. 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 [View Article][PubMed]
     [Google Scholar]
  32. Khajanchi B. K., Sha J., Kozlova E. V., Erova T. E., Suarez G., Sierra J. C., Popov V. L., Horneman A. J., Chopra A. K. ( 2009). N-Acylhomoserine lactones involved in quorum sensing control the type VI secretion system, biofilm formation, protease production, and in vivo virulence in a clinical isolate of Aeromonas hydrophila . Microbiology 155:3518–3531 [View Article][PubMed]
     [Google Scholar]
  33. Khajanchi B. K., Fadl A. A., Borchardt M. A., Berg R. L., Horneman A. J., Stemper M. E., Joseph S. W., Moyer N. P., Sha J., Chopra A. K. ( 2010). Distribution of virulence factors and molecular fingerprinting of Aeromonas species isolates from water and clinical samples: suggestive evidence of water-to-human transmission. Appl Environ Microbiol 76:2313–2325 [View Article][PubMed]
     [Google Scholar]
  34. Kirov S. M. ( 2003). Bacteria that express lateral flagella enable dissection of the multifunctional roles of flagella in pathogenesis. FEMS Microbiol Lett 224:151–159 [View Article][PubMed]
     [Google Scholar]
  35. Kirov S. M., Tassell B. C., Semmler A. B., O’Donovan L. A., Rabaan A. A., Shaw J. G. ( 2002). Lateral flagella and swarming motility in Aeromonas species. J Bacteriol 184:547–555 [View Article][PubMed]
     [Google Scholar]
  36. Kirov S. M., Castrisios M., Shaw J. G. ( 2004). Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infect Immun 72:1939–1945 [View Article][PubMed]
     [Google Scholar]
  37. Kostakioti M., Hadjifrangiskou M., Pinkner J. S., Hultgren S. J. ( 2009). QseC-mediated dephosphorylation of QseB is required for expression of genes associated with virulence in uropathogenic Escherichia coli . Mol Microbiol 73:1020–1031 [View Article][PubMed]
     [Google Scholar]
  38. Kozlova E. V., Popov V. L., Sha J., Foltz S. M., Erova T. E., Agar S. L., Horneman A. J., Chopra A. K. ( 2008). Mutation in the S-ribosylhomocysteinase (luxS) gene involved in quorum sensing affects biofilm formation and virulence in a clinical isolate of Aeromonas hydrophila . Microb Pathog 45:343–354 [View Article][PubMed]
     [Google Scholar]
  39. Kozlova E. V., Khajanchi B. K., Sha J., Chopra A. K. ( 2011). Quorum sensing and c-di-GMP-dependent alterations in gene transcripts and virulence-associated phenotypes in a clinical isolate of Aeromonas hydrophila . Microb Pathog 50:213–223 [View Article][PubMed]
     [Google Scholar]
  40. Krovacek K., Pasquale V., Baloda S. B., Soprano V., Conte M., Dumontet S. ( 1994). Comparison of putative virulence factors in Aeromonas hydrophila strains isolated from the marine environment and human diarrheal cases in southern Italy. Appl Environ Microbiol 60:1379–1382[PubMed]
     [Google Scholar]
  41. Leung K. Y., Stevenson R. M. ( 1988). Tn5-induced protease-deficient strains of Aeromonas hydrophila with reduced virulence for fish. Infect Immun 56:2639–2644[PubMed]
     [Google Scholar]
  42. Moreira C. G., Palmer K., Whiteley M., Sircili M. P., Trabulsi L. R., Castro A. F., Sperandio V. ( 2006). Bundle-forming pili and EspA are involved in biofilm formation by enteropathogenic Escherichia coli . J Bacteriol 188:3952–3961 [View Article][PubMed]
     [Google Scholar]
  43. Moreira C. G., Weinshenker D., Sperandio V. ( 2010). QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo . Infect Immun 78:914–926 [View Article][PubMed]
     [Google Scholar]
  44. Novak E. A., Shao H., Daep C. A., Demuth D. R. ( 2010). Autoinducer-2 and QseC control biofilm formation and in vivo virulence of Aggregatibacter actinomycetemcomitans . Infect Immun 78:2919–2926 [View Article][PubMed]
     [Google Scholar]
  45. O’Toole G. A., Kolter R. ( 1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304 [View Article][PubMed]
     [Google Scholar]
  46. Oggioni M. R., Trappetti C., Kadioglu A., Cassone M., Iannelli F., Ricci S., Andrew P. W., Pozzi G. ( 2006). Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis. Mol Microbiol 61:1196–1210 [View Article][PubMed]
     [Google Scholar]
  47. Petersen F. C., Ahmed N. A., Naemi A., Scheie A. A. ( 2006). LuxS-mediated signalling in Streptococcus anginosus and its role in biofilm formation. Antonie van Leeuwenhoek 90:109–121 [View Article][PubMed]
     [Google Scholar]
  48. Presley S. M., Rainwater T. R., Austin G. P., Platt S. G., Zak J. C., Cobb G. P., Marsland E. J., Tian K., Zhang B. & other authors ( 2006). Assessment of pathogens and toxicants in New Orleans, LA, following Hurricane Katrina. Environ Sci Technol 40:468–474 [View Article][PubMed]
     [Google Scholar]
  49. Rasko D. A., Moreira C. G., Li R., Reading N. C., Ritchie J. M., Waldor M. K., Williams N., Taussig R., Wei S. & other authors ( 2008). Targeting QseC signaling and virulence for antibiotic development. Science 321:1078–1080 [View Article][PubMed]
     [Google Scholar]
  50. Römling U., Simm R. ( 2009). Prevailing concepts of c-di-GMP signaling. Contrib Microbiol 16:161–181 [View Article][PubMed]
     [Google Scholar]
  51. Sakai D. K. ( 1985). Loss of virulence in a protease-deficient mutant of Aeromonas salmonicida . Infect Immun 48:146–152[PubMed]
     [Google Scholar]
  52. Seshadri R., Joseph S. W., Chopra A. K., Sha J., Shaw J., Graf J., Haft D., Wu M., Ren Q. & other authors ( 2006). Genome sequence of Aeromonas hydrophila ATCC 7966T: Jack of all trades. J Bacteriol 188:8272–8282 [View Article][PubMed]
     [Google Scholar]
  53. Sha J., Kozlova E. V., Chopra A. K. ( 2002). Role of various enterotoxins in Aeromonas hydrophila-induced gastroenteritis: generation of enterotoxin gene-deficient mutants and evaluation of their enterotoxic activity. Infect Immun 70:1924–1935 [View Article][PubMed]
     [Google Scholar]
  54. Sha J., Kozlova E. V., Fadl A. A., Olano J. P., Houston C. W., Peterson J. W., Chopra A. K. ( 2004). Molecular characterization of a glucose-inhibited division gene, gidA, that regulates cytotoxic enterotoxin of Aeromonas hydrophila . Infect Immun 72:1084–1095 [View Article][PubMed]
     [Google Scholar]
  55. Sha J., Wang S. F., Suarez G., Sierra J. C., Fadl A. A., Erova T. E., Foltz S. M., Khajanchi B. K., Silver A. & other authors ( 2007). Further characterization of a type III secretion system (T3SS) and of a new effector protein from a clinical isolate of Aeromonas hydrophila – Part I. Microb Pathog 43:127–146 [View Article][PubMed]
     [Google Scholar]
  56. Sierra J. C., Suarez G., Sha J., Foltz S. M., Popov V. L., Galindo C. L., Garner H. R., Chopra A. K. ( 2007). Biological characterization of a new type III secretion system effector from a clinical isolate of Aeromonas hydrophila – Part II. Microb Pathog 43:147–160 [View Article][PubMed]
     [Google Scholar]
  57. Sierra J. C., Suarez G., Sha J., Baze W. B., Foltz S. M., Chopra A. K. ( 2010). Unraveling the mechanism of action of a new type III secretion system effector AexU from Aeromonas hydrophila . Microb Pathog 49:122–134 [View Article][PubMed]
     [Google Scholar]
  58. Singh R., Paul D., Jain R. K. ( 2006). Biofilms: implications in bioremediation. Trends Microbiol 14:389–397 [View Article][PubMed]
     [Google Scholar]
  59. Sperandio V., Torres A. G., Kaper J. B. ( 2002). Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli . Mol Microbiol 43:809–821 [View Article][PubMed]
     [Google Scholar]
  60. Suarez G., Sierra J. C., Sha J., Wang S., Erova T. E., Fadl A. A., Foltz S. M., Horneman A. J., Chopra A. K. ( 2008). Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila . Microb Pathog 44:344–361 [View Article][PubMed]
     [Google Scholar]
  61. Suarez G., Sierra J. C., Erova T. E., Sha J., Horneman A. J., Chopra A. K. ( 2010a). A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J Bacteriol 192:155–168 [View Article][PubMed]
     [Google Scholar]
  62. Suarez G., Sierra J. C., Kirtley M. L., Chopra A. K. ( 2010b). Role of Hcp, a type 6 secretion system effector, of Aeromonas hydrophila in modulating activation of host immune cells. Microbiology 156:3678–3688 [View Article][PubMed]
     [Google Scholar]
  63. Swift S., Lynch M. J., Fish L., Kirke D. F., Tomás J. M., Stewart G. S., Williams P. ( 1999). Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila . Infect Immun 67:5192–5199[PubMed]
     [Google Scholar]
  64. Vila J., Ruiz J., Gallardo F., Vargas M., Soler L., Figueras M. J., Gascon J. ( 2003). Aeromonas spp. and traveler’s diarrhea: clinical features and antimicrobial resistance. Emerg Infect Dis 9:552–555[PubMed] [CrossRef]
     [Google Scholar]
  65. Waldor M. K., Sperandio V. ( 2007). Adrenergic regulation of bacterial virulence. J Infect Dis 195:1248–1249 [View Article][PubMed]
     [Google Scholar]
  66. Walters M., Sperandio V. ( 2006). Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli . Infect Immun 74:5445–5455 [View Article][PubMed]
     [Google Scholar]
  67. Walters M., Sircili M. P., Sperandio V. ( 2006). AI-3 synthesis is not dependent on luxS in Escherichia coli . J Bacteriol 188:5668–5681 [View Article][PubMed]
     [Google Scholar]
  68. Wang X., Wang Q., Yang M., Xiao J., Liu Q., Wu H., Zhang Y. ( 2011). QseBC controls flagellar motility, fimbrial hemagglutination and intracellular virulence in fish pathogen Edwardsiella tarda . Fish Shellfish Immunol 30:944–953 [View Article][PubMed]
     [Google Scholar]
  69. Xu X. J., Ferguson M. R., Popov V. L., Houston C. W., Peterson J. W., Chopra A. K. ( 1998). Role of a cytotoxic enterotoxin in Aeromonas-mediated infections: development of transposon and isogenic mutants. Infect Immun 66:3501–3509[PubMed]
     [Google Scholar]
  70. Zhu J., Mekalanos J. J. ( 2003). Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae . Dev Cell 5:647–656 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.051805-0
Loading
The two-component QseBC signalling system regulates in vitro and in vivo virulence of Aeromonas hydrophila
Microbiology 158, 259 (2012); https://doi.org/10.1099/mic.0.051805-0
/content/journal/micro/10.1099/mic.0.051805-0
/content/journal/micro/10.1099/mic.0.051805-0
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