Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1983 Mar;153(3):1187–1195. doi: 10.1128/jb.153.3.1187-1195.1983

Adenylate cyclase is required for chemotaxis to phosphotransferase system sugars by Escherichia coli.

R A Black, A C Hobson, J Adler
PMCID: PMC221762  PMID: 6298178

Abstract

We report that in Escherichia coli, chemotaxis to sugars transported by the phosphotransferase system is mediated by adenylate cyclase, the nucleotide cyclase linked to the phosphotransferase system. We conclude that adenylate cyclase is required in this chemotaxis pathway because mutations in the cyclase gene (cya) eliminate or impair the response to phosphotransferase system sugars, even though other components of the phosphotransferase system known to be required for the detection of these sugars are relatively unaffected by such mutations. Moreover, merely supplying the mutant bacteria with the products of this enzyme, cyclic AMP and cyclic GMP, does not restore the chemotactic response. Because a residual chemotactic response is observed in certain strains with residual cyclic GMP synthesis but no cyclic AMP synthesis, it appears that the guanylate cyclase activity rather than the adenylate cyclase activity of the enzyme may be required for chemotaxis to sugars transported by the phosphotransferase system. Mutations in the cyclic nucleotide phosphodiesterase gene, which increase the level of both cyclic AMP and cyclic GMP, also reduce chemotaxis to these sugars. Therefore, it appears that control of the level of a cyclic nucleotide is critical for the chemotactic response to phosphotransferase system sugars.

Full text

PDF
1188

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. Adler J. Chemotaxis in bacteria. Science. 1966 Aug 12;153(3737):708–716. doi: 10.1126/science.153.3737.708. [DOI] [PubMed] [Google Scholar]
  3. Adler J., Epstein W. Phosphotransferase-system enzymes as chemoreceptors for certain sugars in Escherichia coli chemotaxis. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2895–2899. doi: 10.1073/pnas.71.7.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Adler J., Hazelbauer G. L., Dahl M. M. Chemotaxis toward sugars in Escherichia coli. J Bacteriol. 1973 Sep;115(3):824–847. doi: 10.1128/jb.115.3.824-847.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Alexander J. K. Suppression of defects in cyclic adenosine 3',5'-monophosphate metabolism in Escherichia coli. J Bacteriol. 1980 Oct;144(1):205–209. doi: 10.1128/jb.144.1.205-209.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Alper M. D., Ames B. N. Cyclic 3', 5'-adenosine monophosphate phosphodiesterase mutants of Salmonella typhimurium. J Bacteriol. 1975 Jun;122(3):1081–1090. doi: 10.1128/jb.122.3.1081-1090.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Black R. A., Hobson A. C., Adler J. Involvement of cyclic GMP in intracellular signaling in the chemotactic response of Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3879–3883. doi: 10.1073/pnas.77.7.3879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brickman E., Soll L., Beckwith J. Genetic characterization of mutations which affect catabolite-sensitive operons in Escherichia coli, including deletions of the gene for adenyl cyclase. J Bacteriol. 1973 Nov;116(2):582–587. doi: 10.1128/jb.116.2.582-587.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Castro L., Feucht B. U., Morse M. L., Saier M. H., Jr Regulation of carbohydrate permeases and adenylate cyclase in Escherichia coli. Studies with mutant strains in which enzyme I of the phosphoenolpyruvate:sugar phosphotransferase system is thermolabile. J Biol Chem. 1976 Sep 25;251(18):5522–5527. [PubMed] [Google Scholar]
  10. Dills S. S., Apperson A., Schmidt M. R., Saier M. H., Jr Carbohydrate transport in bacteria. Microbiol Rev. 1980 Sep;44(3):385–418. doi: 10.1128/mr.44.3.385-418.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Epstein W., Rothman-Denes L. B., Hesse J. Adenosine 3':5'-cyclic monophosphate as mediator of catabolite repression in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2300–2304. doi: 10.1073/pnas.72.6.2300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Feucht B. U., Saier M. H., Jr Fine control of adenylate cyclase by the phosphoenolpyruvate:sugar phosphotransferase systems in Escherichia coli and Salmonella typhimurium. J Bacteriol. 1980 Feb;141(2):603–610. doi: 10.1128/jb.141.2.603-610.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harwood J. P., Gazdar C., Prasad C., Peterkofsky A., Curtis S. J., Epstein W. Involvement of the glucose enzymes II of the sugar phosphotransferase system in the regulation of adenylate cyclase by glucose in Escherichia coli. J Biol Chem. 1976 Apr 25;251(8):2462–2468. [PubMed] [Google Scholar]
  15. Harwood J. P., Peterkofsky A. Glucose-sensitive adenylate cyclase in toluene-treated cells of Escherichia coli B. J Biol Chem. 1975 Jun 25;250(12):4656–4662. [PubMed] [Google Scholar]
  16. Hobson A. C., Black R. A., Adler J. Control of bacterial motility in chemotaxis. Symp Soc Exp Biol. 1982;35:105–121. [PubMed] [Google Scholar]
  17. Joseph E., Bernsley C., Guiso N., Ullmann A. Multiple regulation of the activity of adenylate cyclase in Escherichia coli. Mol Gen Genet. 1982;185(2):262–268. doi: 10.1007/BF00330796. [DOI] [PubMed] [Google Scholar]
  18. Krishnan N., Krishna G. A simple and sensitive assay for guanylate cyclase. Anal Biochem. 1976 Jan;70(1):18–31. doi: 10.1016/s0003-2697(76)80043-7. [DOI] [PubMed] [Google Scholar]
  19. Lengeler J., Auburger A. M., Mayer R., Pecher A. The phosphoenolpyruvate-dependent carbohydrate: phosphotransferase system enzymes II as chemoreceptors in chemotaxis of Escherichia coli K 12. Mol Gen Genet. 1981;183(1):163–170. doi: 10.1007/BF00270156. [DOI] [PubMed] [Google Scholar]
  20. Lengeler J. Mutations affecting transport of the hexitols D-mannitol, D-glucitol, and galactitol in Escherichia coli K-12: isolation and mapping. J Bacteriol. 1975 Oct;124(1):26–38. doi: 10.1128/jb.124.1.26-38.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Macchia V., Varrone S., Weissbach H., Miller D. L. Guanylate cyclase in Escherichia coli. Purification and properties. J Biol Chem. 1975 Aug 25;250(16):6214–6217. [PubMed] [Google Scholar]
  22. Mesibov R., Adler J. Chemotaxis toward amino acids in Escherichia coli. J Bacteriol. 1972 Oct;112(1):315–326. doi: 10.1128/jb.112.1.315-326.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Niwano M., Taylor B. L. Novel sensory adaptation mechanism in bacterial chemotaxis to oxygen and phosphotransferase substrates. Proc Natl Acad Sci U S A. 1982 Jan;79(1):11–15. doi: 10.1073/pnas.79.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Parkinson J. S., Revello P. T. Sensory adaptation mutants of E. coli. Cell. 1978 Dec;15(4):1221–1230. doi: 10.1016/0092-8674(78)90048-x. [DOI] [PubMed] [Google Scholar]
  25. Perlman R. L., Pastan I. Pleiotropic deficiency of carbohydrate utilization in an adenyl cyclase deficient mutant of Escherichia coli. Biochem Biophys Res Commun. 1969 Sep 24;37(1):151–157. doi: 10.1016/0006-291x(69)90893-6. [DOI] [PubMed] [Google Scholar]
  26. Peterkofsky A., Gazdar C. Glucose inhibition of adenylate cyclase in intact cells of Escherichia coli B. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2324–2328. doi: 10.1073/pnas.71.6.2324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Peterkofsky A., Gazdar C. Interaction of enzyme I of the phosphoenolpyruvate:sugar phosphotransferase system with adenylate cyclase of Escherichia coli. Proc Natl Acad Sci U S A. 1975 Aug;72(8):2920–2924. doi: 10.1073/pnas.72.8.2920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Postma P. W., Roseman S. The bacterial phosphoenolpyruvate: sugar phosphotransferase system. Biochim Biophys Acta. 1976 Dec 14;457(3-4):213–257. doi: 10.1016/0304-4157(76)90001-0. [DOI] [PubMed] [Google Scholar]
  29. Rephaeli A. W., Saier M. H., Jr Regulation of genes coding for enzyme constituents of the bacterial phosphotransferase system. J Bacteriol. 1980 Feb;141(2):658–663. doi: 10.1128/jb.141.2.658-663.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rollins C. M., Dahlquist F. W. Methylation of chemotaxis-specific proteins in Escherichia coli cells permeable to S-adenosylmethionine. Biochemistry. 1980 Sep 30;19(20):4627–4632. doi: 10.1021/bi00561a014. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Saier M. H., Jr, Feucht B. U. Coordinate regulation of adenylate cyclase and carbohydrate permeases by the phosphoenolpyruvate:sugar phosphotransferase system in Salmonella typhimurium. J Biol Chem. 1975 Sep 10;250(17):7078–7080. [PubMed] [Google Scholar]
  33. Saier M. H., Jr, Feucht B. U., Hofstadter L. J. Regulation of carbohydrate uptake and adenylate cyclase activity mediated by the enzymes II of the phosphoenolpyruvate: sugar phosphotransferase system in Escherichia coli. J Biol Chem. 1976 Feb 10;251(3):883–892. [PubMed] [Google Scholar]
  34. 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]
  35. Silverman M., Simon M. Characterization of Escherichia coli flagellar mutants that are insensitive to catabolite repression. J Bacteriol. 1974 Dec;120(3):1196–1203. doi: 10.1128/jb.120.3.1196-1203.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. Tao M., Huberman A. Some properties of Escherichia coli adenyl cyclase. Arch Biochem Biophys. 1970 Nov;141(1):236–240. doi: 10.1016/0003-9861(70)90127-x. [DOI] [PubMed] [Google Scholar]
  39. Thompson W. J., Brooker G., Appleman M. M. Assay of cyclic nucleotide phosphodiesterases with radioactive substrates. Methods Enzymol. 1974;38:205–212. doi: 10.1016/0076-6879(74)38033-0. [DOI] [PubMed] [Google Scholar]
  40. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  41. Yokota T., Gots J. S. Requirement of adenosine 3', 5'-cyclic phosphate for flagella formation in Escherichia coli and Salmonella typhimurium. J Bacteriol. 1970 Aug;103(2):513–516. doi: 10.1128/jb.103.2.513-516.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES