Skip to main content
PMC home page
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
. 1980 Jul;77(7):3879–3883. doi: 10.1073/pnas.77.7.3879

Involvement of cyclic GMP in intracellular signaling in the chemotactic response of Escherichia coli.

R A Black, A C Hobson, J Adler
PMCID: PMC349730  PMID: 6253997

Abstract

The intracellular signal that produces changes in swimming behavior when bacteria encounter attractants or repellents has not previously been identified. We suggest, based on the following lines of evidence, that cyclic GMP (cGMP) is involved in this signaling process in chemotaxis by Escherichia coli. (i) The addition of attractants to bacteria causes a transient increase in the intracellular level of cGMP, whereas a repellent stimulus decreases the level transiently. These changes do not generally occur in a mutant lacking chemotaxis-specific proteins. (ii) In the absence of chemoeffectors, both addition of cGMP to bacteria and reducing the intracellular cGMP level produce changes in swimming behavior, and a mutant with an abnormal swimming pattern has an altered intracellular cGMP level. (iii) cGMP modulates the demethylation reaction responsible for adaptation to stimuli. (iv) Mutants defective in components of the adaptation system have altered cGMP metabolism.

Full text

PDF
3880

Selected References

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

  1. Adler J. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol. 1973 Jan;74(1):77–91. doi: 10.1099/00221287-74-1-77. [DOI] [PubMed] [Google Scholar]
  2. Berg H. C. Chemotaxis in bacteria. Annu Rev Biophys Bioeng. 1975;4(00):119–136. doi: 10.1146/annurev.bb.04.060175.001003. [DOI] [PubMed] [Google Scholar]
  3. Bernlohr R. W., Haddox M. K., Goldberg N. D. Cyclic guanosine 3':5'-monophosphate in Escherichia coli and Bacillus lichenformis. J Biol Chem. 1974 Jul 10;249(13):4329–4331. [PubMed] [Google Scholar]
  4. Cook W. R., Kalb V. F., Jr, Peace A. A., Bernlohr R. W. Is cyclic guanosine 3',5'-monophosphate a cell cycle regulator? J Bacteriol. 1980 Mar;141(3):1450–1453. doi: 10.1128/jb.141.3.1450-1453.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dobrogosz W. J., Hamilton P. B. The role of cyclic AMP in chemotaxis in Escherichia coli. Biochem Biophys Res Commun. 1971 Jan 22;42(2):202–207. doi: 10.1016/0006-291x(71)90088-x. [DOI] [PubMed] [Google Scholar]
  6. Goldberg N. D., Haddox M. K. Cyclic GMP metabolism and involvement in biological regulation. Annu Rev Biochem. 1977;46:823–896. doi: 10.1146/annurev.bi.46.070177.004135. [DOI] [PubMed] [Google Scholar]
  7. Goldenbaum P. E., Hall G. A. Transport of cyclic adenosine 3',5'-monophosphate across Escherichia coli vesicle membranes. J Bacteriol. 1979 Nov;140(2):459–467. doi: 10.1128/jb.140.2.459-467.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gonzalez J. E., Peterkofsky A. Diverse directional changes of cGMP relative to cAMP in E. coli. Biochem Biophys Res Commun. 1975 Nov 3;67(1):190–197. doi: 10.1016/0006-291x(75)90301-0. [DOI] [PubMed] [Google Scholar]
  9. Goy M. F., Springer M. S., Adler J. Failure of sensory adaptation in bacterial mutants that are defective in a protein methylation reaction. Cell. 1978 Dec;15(4):1231–1240. doi: 10.1016/0092-8674(78)90049-1. [DOI] [PubMed] [Google Scholar]
  10. Greengard P. Phosphorylated proteins as physiological effectors. Science. 1978 Jan 13;199(4325):146–152. doi: 10.1126/science.22932. [DOI] [PubMed] [Google Scholar]
  11. Hayashi H., Koiwai O., Kozuka M. Studies on bacterial chemotaxis. II. Effect of cheB and cheZ mutations on the methylation of methyl-accepting chemotaxis protein of Escherichia coli. J Biochem. 1979 May;85(5):1213–1223. [PubMed] [Google Scholar]
  12. Hubbell W. L., Bownds M. D. Visual transduction in vertebrate photoreceptors. Annu Rev Neurosci. 1979;2:17–34. doi: 10.1146/annurev.ne.02.030179.000313. [DOI] [PubMed] [Google Scholar]
  13. Kleene S. J., Hobson A. C., Adler J. Attractants and repellents influence methylation and demethylation of methyl-accepting chemotaxis proteins in an extract of Escherichia coli. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6309–6313. doi: 10.1073/pnas.76.12.6309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Macnab R. M., Koshland D. E., Jr The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2509–2512. doi: 10.1073/pnas.69.9.2509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mato J. M., Krens F. A., van Haastert P. J., Konijn T. M. 3':5'-cyclic AMP-dependent 3':5'-cyclic GMP accumulation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2348–2351. doi: 10.1073/pnas.74.6.2348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Parkinson J. S. Complementation analysis and deletion mapping of Escherichia coli mutants defective in chemotaxis. J Bacteriol. 1978 Jul;135(1):45–53. doi: 10.1128/jb.135.1.45-53.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sabourin D., Beckwith J. Deletion of the Escherichia coli crp gene. J Bacteriol. 1975 Apr;122(1):338–340. doi: 10.1128/jb.122.1.338-340.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Shibuya M., Takebe Y., Kaziro Y. A possible involvement of cya gene in the synthesis of cyclic guanosine 3':5'-monophosphate in E. coli. Cell. 1977 Oct;12(2):521–528. doi: 10.1016/0092-8674(77)90128-3. [DOI] [PubMed] [Google Scholar]
  19. Silverman M., Simon M. Identification of polypeptides necessary for chemotaxis in Escherichia coli. J Bacteriol. 1977 Jun;130(3):1317–1325. doi: 10.1128/jb.130.3.1317-1325.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Springer M. S., Goy M. F., Adler J. Protein methylation in behavioural control mechanisms and in signal transduction. Nature. 1979 Jul 26;280(5720):279–284. doi: 10.1038/280279a0. [DOI] [PubMed] [Google Scholar]
  21. Taylor A. L., Trotter C. D. Revised linkage map of Escherichia coli. Bacteriol Rev. 1967 Dec;31(4):332–353. doi: 10.1128/br.31.4.332-353.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Toews M. L., Adler J. Methanol formation in vivo from methylated chemotaxis proteins in Escherichia coli. J Biol Chem. 1979 Mar 25;254(6):1761–1764. [PubMed] [Google Scholar]
  23. Toews M. L., Goy M. F., Springer M. S., Adler J. Attractants and repellents control demethylation of methylated chemotaxis proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5544–5548. doi: 10.1073/pnas.76.11.5544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wurster B., Schubiger K., Wick U., Gerisch G. Cyclic GMP in Dictyostelium discoideum, Oscillations and pulses in response to folic acid and cyclic AMP signals. FEBS Lett. 1977 Apr 15;76(2):141–144. doi: 10.1016/0014-5793(77)80139-7. [DOI] [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