1887

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Volume 157, Issue 5

Participation of CheR and CheB in the chemosensory response of Free

Abstract

is a leading cause of bacterial gastroenteritis in humans and a commensal bacterium of the intestinal tracts of animals, especially poultry. Chemotaxis is an important determinant for chicken colonization of . Adaptation has a crucial role in the gradient-sensing mechanism that underlies chemotaxis. The genome sequence of reveals the presence of genes encoding putative adaptation proteins, CheB and CheR. In-frame deletions of , and were constructed and the chemosensory behaviour of the resultant mutants was examined on swarm plates. CheB and CheR proteins significantly influence chemotaxis but are not essential for this behaviour to occur. Increased mobility of two methyl-accepting chemotaxis proteins (MCPs), DocC and Tlp1, during SDS-PAGE was detected in the mutants lacking functional CheB in the presence of CheR, presumably resulting from stable methylation of receptors. studies using tissue culture revealed that deletion of resulted in hyperadherent and hyperinvasive phenotypes, while deletion of resulted in nonadherent, noninvasive phenotypes. Furthermore, the Δmutant showed significantly reduced ability to colonize chick caeca. Our data suggest that modification of chemoreceptors by the CheBR system is involved in regulation of chemotaxis in although CheB is apparently not controlled by phosphorylation.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Funding
This study was supported by the:
  • Japan Society for the Promotion of Science (Award 21580381)
© 2011 SGM
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2011-05-01
2024-04-20
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References

  1. Abremski K., Hoess R. ( 1984). Bacteriophage P1 site-specific recombination. Purification and properties of the Cre recombinase protein. J Biol Chem 259:1509–1514[PubMed]
     [Google Scholar]
  2. Altekruse S. F., Stern N. J., Fields P. I., Swerdlow D. L. ( 1999). Campylobacter jejuni–an emerging foodborne pathogen. Emerg Infect Dis 5:28–35 [View Article][PubMed]
     [Google Scholar]
  3. Beery J. T., Hugdahl M. B., Doyle M. P. ( 1988). Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni . Appl Environ Microbiol 54:2365–2370[PubMed]
     [Google Scholar]
  4. Bibikov S. I., Miller A. C., Gosink K. K., Parkinson J. S. ( 2004). Methylation-independent aerotaxis mediated by the Escherichia coli Aer protein. J Bacteriol 186:3730–3737 [View Article][PubMed]
     [Google Scholar]
  5. Black R. E., Levine M. M., Clements M. L., Hughes T. P., Blaser M. J. ( 1988). Experimental Campylobacter jejuni infection in humans. J Infect Dis 157:472–479[PubMed] [CrossRef]
     [Google Scholar]
  6. Bunn M. W., Ordal G. W. ( 2004). Receptor conformational changes enhance methylesterase activity during chemotaxis by Bacillus subtilis . Mol Microbiol 51:721–728 [View Article][PubMed]
     [Google Scholar]
  7. Chang C., Miller J. F. ( 2006). Campylobacter jejuni colonization of mice with limited enteric flora. Infect Immun 74:5261–5271 [View Article][PubMed]
     [Google Scholar]
  8. del Rocio Leon-Kempis M., Guccione E., Mulholland F., Williamson M. P., Kelly D. J. ( 2006). The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol Microbiol 60:1262–1275 [View Article][PubMed]
     [Google Scholar]
  9. Elliott K. T., Zhulin I. B., Stuckey J. A., DiRita V. J. ( 2009). Conserved residues in the HAMP domain define a new family of proposed bipartite energy taxis receptors. J Bacteriol 191:375–387 [View Article][PubMed]
     [Google Scholar]
  10. Everest P. H., Goossens H., Butzler J. P., Lloyd D., Knutton S., Ketley J. M., Williams P. H. ( 1992). Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli . J Med Microbiol 37:319–325 [View Article][PubMed]
     [Google Scholar]
  11. Flanagan R. C., Neal-McKinney J. M., Dhillon A. S., Miller W. G., Konkel M. E. ( 2009). Examination of Campylobacter jejuni putative adhesins leads to the identification of a new protein, designated FlpA, required for chicken colonization. Infect Immun 77:2399–2407 [View Article][PubMed]
     [Google Scholar]
  12. Hartley-Tassell L. E., Shewell L. K., Day C. J., Wilson J. C., Sandhu R., Ketley J. M., Korolik V. ( 2010). Identification and characterization of the aspartate chemosensory receptor of Campylobacter jejuni . Mol Microbiol 75:710–730 [View Article][PubMed]
     [Google Scholar]
  13. Hendrixson D. R. ( 2006). A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol Microbiol 61:1646–1659 [View Article][PubMed]
     [Google Scholar]
  14. Hendrixson D. R., DiRita V. J. ( 2004). Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52:471–484 [View Article][PubMed]
     [Google Scholar]
  15. Hendrixson D. R., Akerley B. J., DiRita V. J. ( 2001). Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40:214–224 [View Article][PubMed]
     [Google Scholar]
  16. Horrocks S. M., Anderson R. C., Nisbet D. J., Ricke S. C. ( 2009). Incidence and ecology of Campylobacter jejuni and coli in animals. Anaerobe 15:18–25 [View Article][PubMed]
     [Google Scholar]
  17. Jiménez-Pearson M. A., Delany I., Scarlato V., Beier D. ( 2005). Phosphate flow in the chemotactic response system of Helicobacter pylori . Microbiology 151:3299–3311 [View Article][PubMed]
     [Google Scholar]
  18. Kakuda T., DiRita V. J. ( 2006). Cj1496c encodes a Campylobacter jejuni glycoprotein that influences invasion of human epithelial cells and colonization of the chick gastrointestinal tract. Infect Immun 74:4715–4723 [View Article][PubMed]
     [Google Scholar]
  19. Korlath J. A., Osterholm M. T., Judy L. A., Forfang J. C., Robinson R. A. ( 1985). A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152:592–596[PubMed] [CrossRef]
     [Google Scholar]
  20. Lara-Tejero M., Galán J. E. ( 2000). A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 290:354–357 [View Article][PubMed]
     [Google Scholar]
  21. Lupas A., Stock J. ( 1989). Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. J Biol Chem 264:17337–17342[PubMed]
     [Google Scholar]
  22. Marchant J., Wren B., Ketley J. ( 2002). Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. Trends Microbiol 10:155–159 [View Article][PubMed]
     [Google Scholar]
  23. Miller L. D., Russell M. H., Alexandre G. ( 2009). Diversity in bacterial chemotactic responses and niche adaptation. Adv Appl Microbiol 66:53–75 [View Article][PubMed]
     [Google Scholar]
  24. Novik V., Hofreuter D., Galán J. E. ( 2010). Identification of Campylobacter jejuni genes involved in its interaction with epithelial cells. Infect Immun 78:3540–3553 [View Article][PubMed]
     [Google Scholar]
  25. Pei Z., Burucoa C., Grignon B., Baqar S., Huang X. Z., Kopecko D. J., Bourgeois A. L., Fauchere J. L., Blaser M. J. ( 1998). Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect Immun 66:938–943[PubMed]
     [Google Scholar]
  26. Rao C. V., Ordal G. W. ( 2009). The molecular basis of excitation and adaptation during chemotactic sensory transduction in bacteria. Contrib Microbiol 16:33–64 [View Article][PubMed]
     [Google Scholar]
  27. Rao C. V., Glekas G. D., Ordal G. W. ( 2008). The three adaptation systems of Bacillus subtilis chemotaxis. Trends Microbiol 16:480–487 [View Article][PubMed]
     [Google Scholar]
  28. Shiomi D., Zhulin I. B., Homma M., Kawagishi I. ( 2002). Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J Biol Chem 277:42325–42333 [View Article][PubMed]
     [Google Scholar]
  29. Sockett R. E., Armitage J. P., Evans M. C. ( 1987). Methylation-independent and methylation-dependent chemotaxis in Rhodobacter sphaeroides and Rhodospirillum rubrum . J Bacteriol 169:5808–5814[PubMed]
     [Google Scholar]
  30. Stephens B. B., Loar S. N., Alexandre G. ( 2006). Role of CheB and CheR in the complex chemotactic and aerotactic pathway of Azospirillum brasilense . J Bacteriol 188:4759–4768 [View Article][PubMed]
     [Google Scholar]
  31. Stock J. B., Clarke S., Koshland D. E. Jr ( 1984). The protein carboxylmethyltransferase involved in Escherichia coli and Salmonella typhimurium chemotaxis. Methods Enzymol 106:310–321 [View Article][PubMed]
     [Google Scholar]
  32. Szurmant H., Ordal G. W. ( 2004). Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68:301–319 [View Article][PubMed]
     [Google Scholar]
  33. Takata T., Fujimoto S., Amako K. ( 1992). Isolation of nonchemotactic mutants of Campylobacter jejuni and their colonization of the mouse intestinal tract. Infect Immun 60:3596–3600[PubMed]
     [Google Scholar]
  34. Vladimirov N., Sourjik V. ( 2009). Chemotaxis: how bacteria use memory. Biol Chem 390:1097–1104 [View Article][PubMed]
     [Google Scholar]
  35. Wassenaar T. M., Blaser M. J. ( 1999). Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1:1023–1033 [View Article][PubMed]
     [Google Scholar]
  36. Weiner M. P., Costa G. L., Schoettlin W., Cline J., Mathur E., Bauer J. C. ( 1994). Site-directed mutagenesis of double-stranded DNA by the polymerase chain reaction. Gene 151:119–123 [View Article][PubMed]
     [Google Scholar]
  37. West A. H., Martinez-Hackert E., Stock A. M. ( 1995). Crystal structure of the catalytic domain of the chemotaxis receptor methylesterase, CheB. J Mol Biol 250:276–290 [View Article][PubMed]
     [Google Scholar]
  38. Wiesner R. S., Hendrixson D. R., DiRita V. J. ( 2003). Natural transformation of Campylobacter jejuni requires components of a type II secretion system. J Bacteriol 185:5408–5418 [View Article][PubMed]
     [Google Scholar]
  39. Yao R., Burr D. H., Guerry P. ( 1997). CheY-mediated modulation of Campylobacter jejuni virulence. Mol Microbiol 23:1021–1031 [View Article][PubMed]
     [Google Scholar]
  40. Yonekawa H., Hayashi H., Parkinson J. S. ( 1983). Requirement of the cheB function for sensory adaptation in Escherichia coli . J Bacteriol 156:1228–1235[PubMed]
     [Google Scholar]
  41. Zilbauer M., Dorrell N., Wren B. W., Bajaj-Elliott M. ( 2008). Campylobacter jejuni-mediated disease pathogenesis: an update. Trans R Soc Trop Med Hyg 102:123–129 [View Article][PubMed]
     [Google Scholar]
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Participation of CheR and CheB in the chemosensory response of Campylobacter jejuni
Microbiology 157, 1279 (2011); https://doi.org/10.1099/mic.0.047399-0
/content/journal/micro/10.1099/mic.0.047399-0
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