Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1994 May;176(9):2736–2739. doi: 10.1128/jb.176.9.2736-2739.1994

Chemotaxis in Bacillus subtilis requires either of two functionally redundant CheW homologs.

M M Rosario 1, K L Fredrick 1, G W Ordal 1, J D Helmann 1
PMCID: PMC205415  PMID: 8169224

Abstract

We have characterized mutants in a novel gene of Bacillus subtilis, cheV, which encodes a protein homologous to both CheW and CheY. A null mutant in cheV is only slightly defective in capillary and tethered cell assays. However, a double mutant lacking both CheV and CheW has a strong tumble bias, does not respond to addition of attractant, and shows essentially no accumulation in capillary assays. Thus, CheV and CheW appear in part to be functionally redundant. A strain lacking CheW and expressing only the CheW domain of CheV is chemotactic, suggesting that the truncated CheV protein retains in vivo function. We speculate that CheV and CheW function together to couple CheA activation to methyl-accepting chemotaxis protein receptor status and that possible CheA-dependent phosphorylation of CheV contributes to adaptation.

Full text

PDF
2737

Images in this article

2738Image
on p.2738

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berg H. C., Block S. M. A miniature flow cell designed for rapid exchange of media under high-power microscope objectives. J Gen Microbiol. 1984 Nov;130(11):2915–2920. doi: 10.1099/00221287-130-11-2915. [DOI] [PubMed] [Google Scholar]
  2. Berg H. C., Tedesco P. M. Transient response to chemotactic stimuli in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3235–3239. doi: 10.1073/pnas.72.8.3235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bischoff D. S., Ordal G. W. Bacillus subtilis chemotaxis: a deviation from the Escherichia coli paradigm. Mol Microbiol. 1992 Jan;6(1):23–28. doi: 10.1111/j.1365-2958.1992.tb00833.x. [DOI] [PubMed] [Google Scholar]
  4. Bischoff D. S., Ordal G. W. Sequence and characterization of Bacillus subtilis CheB, a homolog of Escherichia coli CheY, and its role in a different mechanism of chemotaxis. J Biol Chem. 1991 Jul 5;266(19):12301–12305. [PubMed] [Google Scholar]
  5. Borkovich K. A., Kaplan N., Hess J. F., Simon M. I. Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1208–1212. doi: 10.1073/pnas.86.4.1208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Borkovich K. A., Simon M. I. The dynamics of protein phosphorylation in bacterial chemotaxis. Cell. 1990 Dec 21;63(6):1339–1348. doi: 10.1016/0092-8674(90)90429-i. [DOI] [PubMed] [Google Scholar]
  7. Bourret R. B., Borkovich K. A., Simon M. I. Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu Rev Biochem. 1991;60:401–441. doi: 10.1146/annurev.bi.60.070191.002153. [DOI] [PubMed] [Google Scholar]
  8. Bourret R. B., Hess J. F., Borkovich K. A., Pakula A. A., Simon M. I. Protein phosphorylation in chemotaxis and two-component regulatory systems of bacteria. J Biol Chem. 1989 May 5;264(13):7085–7088. [PubMed] [Google Scholar]
  9. Bourret R. B., Hess J. F., Simon M. I. Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc Natl Acad Sci U S A. 1990 Jan;87(1):41–45. doi: 10.1073/pnas.87.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fredrick K. L., Helmann J. D. Dual chemotaxis signaling pathways in Bacillus subtilis: a sigma D-dependent gene encodes a novel protein with both CheW and CheY homologous domains. J Bacteriol. 1994 May;176(9):2727–2735. doi: 10.1128/jb.176.9.2727-2735.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fuhrer D. K., Ordal G. W. Bacillus subtilis CheN, a homolog of CheA, the central regulator of chemotaxis in Escherichia coli. J Bacteriol. 1991 Dec;173(23):7443–7448. doi: 10.1128/jb.173.23.7443-7448.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gegner J. A., Graham D. R., Roth A. F., Dahlquist F. W. Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell. 1992 Sep 18;70(6):975–982. doi: 10.1016/0092-8674(92)90247-a. [DOI] [PubMed] [Google Scholar]
  13. Hanlon D. W., Carpenter P. B., Ordal G. W. Influence of attractants and repellents on methyl group turnover on methyl-accepting chemotaxis proteins of Bacillus subtilis and role of CheW. J Bacteriol. 1992 Jul;174(13):4218–4222. doi: 10.1128/jb.174.13.4218-4222.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hanlon D. W., Márquez-Magaña L. M., Carpenter P. B., Chamberlin M. J., Ordal G. W. Sequence and characterization of Bacillus subtilis CheW. J Biol Chem. 1992 Jun 15;267(17):12055–12060. [PubMed] [Google Scholar]
  15. Hess J. F., Oosawa K., Kaplan N., Simon M. I. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell. 1988 Apr 8;53(1):79–87. doi: 10.1016/0092-8674(88)90489-8. [DOI] [PubMed] [Google Scholar]
  16. Kirsch M. L., Peters P. D., Hanlon D. W., Kirby J. R., Ordal G. W. Chemotactic methylesterase promotes adaptation to high concentrations of attractant in Bacillus subtilis. J Biol Chem. 1993 Sep 5;268(25):18610–18616. [PubMed] [Google Scholar]
  17. Kirsch M. L., Zuberi A. R., Henner D., Peters P. D., Yazdi M. A., Ordal G. W. Chemotactic methyltransferase promotes adaptation to repellents in Bacillus subtilis. J Biol Chem. 1993 Dec 5;268(34):25350–25356. [PubMed] [Google Scholar]
  18. Liu J. D., Parkinson J. S. Role of CheW protein in coupling membrane receptors to the intracellular signaling system of bacterial chemotaxis. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8703–8707. doi: 10.1073/pnas.86.22.8703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McNally D. F., Matsumura P. Bacterial chemotaxis signaling complexes: formation of a CheA/CheW complex enhances autophosphorylation and affinity for CheY. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6269–6273. doi: 10.1073/pnas.88.14.6269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ordal G. W., Goldman D. J. Chemotaxis away from uncouplers of oxidative phosphorylation in Bacillus subtilis. Science. 1975 Sep 5;189(4205):802–805. doi: 10.1126/science.808854. [DOI] [PubMed] [Google Scholar]
  21. Stock J. B., Lukat G. S., Stock A. M. Bacterial chemotaxis and the molecular logic of intracellular signal transduction networks. Annu Rev Biophys Biophys Chem. 1991;20:109–136. doi: 10.1146/annurev.bb.20.060191.000545. [DOI] [PubMed] [Google Scholar]
  22. Stock J. B., Surette M. G., McCleary W. R., Stock A. M. Signal transduction in bacterial chemotaxis. J Biol Chem. 1992 Oct 5;267(28):19753–19756. [PubMed] [Google Scholar]
  23. Thoelke M. S., Kirby J. R., Ordal G. W. Novel methyl transfer during chemotaxis in Bacillus subtilis. Biochemistry. 1989 Jun 27;28(13):5585–5589. doi: 10.1021/bi00439a037. [DOI] [PubMed] [Google Scholar]
  24. Ullah A. H., Ordal G. W. In vivo and in vitro chemotactic methylation in Bacillus subtilis. J Bacteriol. 1981 Feb;145(2):958–965. doi: 10.1128/jb.145.2.958-965.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Welch M., Oosawa K., Aizawa S., Eisenbach M. Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8787–8791. doi: 10.1073/pnas.90.19.8787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wolfe A. J., Berg H. C. Migration of bacteria in semisolid agar. Proc Natl Acad Sci U S A. 1989 Sep;86(18):6973–6977. doi: 10.1073/pnas.86.18.6973. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES