Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Aug;87(15):5898–5902. doi: 10.1073/pnas.87.15.5898

FrzE of Myxococcus xanthus is homologous to both CheA and CheY of Salmonella typhimurium.

W R McCleary 1, D R Zusman 1
PMCID: PMC54436  PMID: 2165608

Abstract

Myxococcus xanthus exhibits multicellular development. The "frizzy" (frz) mutants are unable to complete the developmental pathway. Instead of forming fruiting bodies, these mutants form tangled filaments of cells. We have previously shown that four of the frz gene products are homologous to enteric chemotaxis proteins and have proposed that the frz genes constitute a signal-transduction pathway that controls the frequency at which cells reverse their gliding direction. We show here that frzE encodes a protein with a calculated molecular mass of 83 kDa. FrzE is homologous to both CheA and CheY of Salmonella typhimurium, which are members of a family of "two-component response regulators." It is thought that the modulator components autophosphorylate and transfer a phosphate group to their cognate effector components. FrzE contains an unusual (alanine plus proline)-rich region that might constitute a flexible hinge facilitating phosphate transfer between functional domains. We suggest that FrzE is a second messenger that relays information between the signaling protein FrzCD and the gliding motor.

Full text

PDF
5898

Selected References

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

  1. Bibb M. J., Findlay P. R., Johnson M. W. The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene. 1984 Oct;30(1-3):157–166. doi: 10.1016/0378-1119(84)90116-1. [DOI] [PubMed] [Google Scholar]
  2. Blackhart B. D., Zusman D. R. "Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8767–8770. doi: 10.1073/pnas.82.24.8767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blackhart B. D., Zusman D. R. Analysis of the products of the Myxococcus xanthus frz genes. J Bacteriol. 1986 May;166(2):673–678. doi: 10.1128/jb.166.2.673-678.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blackhart B. D., Zusman D. R. Cloning and complementation analysis of the "Frizzy" genes of Myxococcus xanthus. Mol Gen Genet. 1985;198(2):243–254. doi: 10.1007/BF00383002. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. DWORKIN M. Nutritional requirements for vegetative growth of Myxococcus xanthus. J Bacteriol. 1962 Aug;84:250–257. doi: 10.1128/jb.84.2.250-257.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Forst S., Delgado J., Inouye M. Phosphorylation of OmpR by the osmosensor EnvZ modulates expression of the ompF and ompC genes in Escherichia coli. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6052–6056. doi: 10.1073/pnas.86.16.6052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hess J. F., Oosawa K., Matsumura P., Simon M. I. Protein phosphorylation is involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7609–7613. doi: 10.1073/pnas.84.21.7609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Keener J., Kustu S. Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC. Proc Natl Acad Sci U S A. 1988 Jul;85(14):4976–4980. doi: 10.1073/pnas.85.14.4976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Koshland D. E., Jr Biochemistry of sensing and adaptation in a simple bacterial system. Annu Rev Biochem. 1981;50:765–782. doi: 10.1146/annurev.bi.50.070181.004001. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Lupas A., Stock J. Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. J Biol Chem. 1989 Oct 15;264(29):17337–17342. [PubMed] [Google Scholar]
  13. McBride M. J., Weinberg R. A., Zusman D. R. "Frizzy" aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc Natl Acad Sci U S A. 1989 Jan;86(2):424–428. doi: 10.1073/pnas.86.2.424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Miles J. S., Guest J. R., Radford S. E., Perham R. N. Investigation of the mechanism of active site coupling in the pyruvate dehydrogenase multienzyme complex of Escherichia coli by protein engineering. J Mol Biol. 1988 Jul 5;202(1):97–106. doi: 10.1016/0022-2836(88)90522-0. [DOI] [PubMed] [Google Scholar]
  15. Morrison C. E., Zusman D. R. Myxococcus xanthus mutants with temperature-sensitive, stage-specific defects: evidence for independent pathways in development. J Bacteriol. 1979 Dec;140(3):1036–1042. doi: 10.1128/jb.140.3.1036-1042.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Oosawa K., Hess J. F., Simon M. I. Mutants defective in bacterial chemotaxis show modified protein phosphorylation. Cell. 1988 Apr 8;53(1):89–96. doi: 10.1016/0092-8674(88)90490-4. [DOI] [PubMed] [Google Scholar]
  17. Radford S. E., Laue E. D., Perham R. N., Martin S. R., Appella E. Conformational flexibility and folding of synthetic peptides representing an interdomain segment of polypeptide chain in the pyruvate dehydrogenase multienzyme complex of Escherichia coli. J Biol Chem. 1989 Jan 15;264(2):767–775. [PubMed] [Google Scholar]
  18. Sanders D. A., Gillece-Castro B. L., Stock A. M., Burlingame A. L., Koshland D. E., Jr Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J Biol Chem. 1989 Dec 25;264(36):21770–21778. [PubMed] [Google Scholar]
  19. Sanders D. A., Mendez B., Koshland D. E., Jr Role of the CheW protein in bacterial chemotaxis: overexpression is equivalent to absence. J Bacteriol. 1989 Nov;171(11):6271–6278. doi: 10.1128/jb.171.11.6271-6278.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Stibitz S., Aaronson W., Monack D., Falkow S. Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature. 1989 Mar 16;338(6212):266–269. doi: 10.1038/338266a0. [DOI] [PubMed] [Google Scholar]
  21. Stock A. M., Mottonen J. M., Stock J. B., Schutt C. E. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature. 1989 Feb 23;337(6209):745–749. doi: 10.1038/337745a0. [DOI] [PubMed] [Google Scholar]
  22. Stock A., Chen T., Welsh D., Stock J. CheA protein, a central regulator of bacterial chemotaxis, belongs to a family of proteins that control gene expression in response to changing environmental conditions. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1403–1407. doi: 10.1073/pnas.85.5.1403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stock A., Koshland D. E., Jr, Stock J. Homologies between the Salmonella typhimurium CheY protein and proteins involved in the regulation of chemotaxis, membrane protein synthesis, and sporulation. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7989–7993. doi: 10.1073/pnas.82.23.7989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Weinberg R. A., Zusman D. R. Evidence that the Myxococcus xanthus frz genes are developmentally regulated. J Bacteriol. 1989 Nov;171(11):6174–6186. doi: 10.1128/jb.171.11.6174-6186.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zusman D. R. "Frizzy" mutants: a new class of aggregation-defective developmental mutants of Myxococcus xanthus. J Bacteriol. 1982 Jun;150(3):1430–1437. doi: 10.1128/jb.150.3.1430-1437.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES