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. 1983 Dec;156(3):1228–1235. doi: 10.1128/jb.156.3.1228-1235.1983

Requirement of the cheB function for sensory adaptation in Escherichia coli.

H Yonekawa, H Hayashi, J S Parkinson
PMCID: PMC217972  PMID: 6358193

Abstract

The chemotactic behavior of Escherichia coli mutants defective in cheB function, which is required to remove methyl esters from methyl-accepting chemotaxis proteins, was investigated by subjecting swimming or antibody-tethered cells to various attractant chemicals. Two cheB point mutants, one missense and one nonsense, exhibited stimulus response times much longer than did the wild type, but they eventually returned to the prestimulus swimming pattern, indicating that they were not completely defective in sensory adaptation. In contrast, strains deleted for the cheB function showed no evidence of adaptation ability after stimulation. The crucial difference between these strains appeared to be the residual level of cheB-dependent methylesterase activity they contained. Both point mutants showed detectable levels of methanol evolution due to turnover of methyl groups on methyl-accepting chemotaxis protein molecules, whereas the cheB deletion mutant did not. In addition, it was possible to incorporate the methyl label into the methyl-accepting chemotaxis proteins of the point mutants but not into those of the cheB deletion strain. These findings indicate that cheB function is essential for sensory adaptation in Escherichia coli.

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Selected References

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  1. Berg H. C., Anderson R. A. Bacteria swim by rotating their flagellar filaments. Nature. 1973 Oct 19;245(5425):380–382. doi: 10.1038/245380a0. [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. 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]
  4. Goy M. F., Springer M. S., Adler J. Sensory transduction in Escherichia coli: role of a protein methylation reaction in sensory adaptation. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4964–4968. doi: 10.1073/pnas.74.11.4964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Hedblom M. L., Adler J. Genetic and biochemical properties of Escherichia coli mutants with defects in serine chemotaxis. J Bacteriol. 1980 Dec;144(3):1048–1060. doi: 10.1128/jb.144.3.1048-1060.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Khan S., Macnab R. M., DeFranco A. L., Koshland D. E., Jr Inversion of a behavioral response in bacterial chemotaxis: explanation at the molecular level. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4150–4154. doi: 10.1073/pnas.75.9.4150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kleene S. J., Toews M. L., Adler J. Isolation of glutamic acid methyl ester from an Escherichia coli membrane protein involved in chemotaxis. J Biol Chem. 1977 May 25;252(10):3214–3218. [PubMed] [Google Scholar]
  9. Koiwai O., Hayashi H. Studies on bacterial chemotaxis. IV. Interaction of maltose receptor with a membrane-bound chemosensing component. J Biochem. 1979 Jul;86(1):27–34. [PubMed] [Google Scholar]
  10. Kort E. N., Goy M. F., Larsen S. H., Adler J. Methylation of a membrane protein involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3939–3943. doi: 10.1073/pnas.72.10.3939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Larsen S. H., Reader R. W., Kort E. N., Tso W. W., Adler J. Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli. Nature. 1974 May 3;249(452):74–77. doi: 10.1038/249074a0. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Minoshima S., Ohba M., Hayashi H. An in vitro study of the methylation of methyl-accepting chemotaxis protein of Escherichia coli. Construction of the system and effect of mutant proteins on the system. J Biochem. 1981 Feb;89(2):411–420. doi: 10.1093/oxfordjournals.jbchem.a133216. [DOI] [PubMed] [Google Scholar]
  14. Ohba M., Hayashi H. Studies on bacterial chemotaxis. III. Effect of methyl esters on the chemotactic response of Escherichia coli. J Biochem. 1979 May;85(5):1331–1338. [PubMed] [Google Scholar]
  15. 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]
  16. Parkinson J. S., Houts S. E. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J Bacteriol. 1982 Jul;151(1):106–113. doi: 10.1128/jb.151.1.106-113.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Parkinson J. S. cheA, cheB, and cheC genes of Escherichia coli and their role in chemotaxis. J Bacteriol. 1976 May;126(2):758–770. doi: 10.1128/jb.126.2.758-770.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Richarme G. Interaction of the maltose-binding protein with membrane vesicles of Escherichia coli. J Bacteriol. 1982 Feb;149(2):662–667. doi: 10.1128/jb.149.2.662-667.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rollins C., Dahlquist F. W. The methyl-accepting chemotaxis proteins of E. coli: a repellent-stimulated, covalent modification, distinct from methylation. Cell. 1981 Aug;25(2):333–340. doi: 10.1016/0092-8674(81)90051-9. [DOI] [PubMed] [Google Scholar]
  21. Rubik B. A., Koshland D. E., Jr Potentiation, desensitization, and inversion of response in bacterial sensing of chemical stimuli. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2820–2824. doi: 10.1073/pnas.75.6.2820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sherris D., Parkinson J. S. Posttranslational processing of methyl-accepting chemotaxis proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6051–6055. doi: 10.1073/pnas.78.10.6051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Silverman M., Simon M. Flagellar rotation and the mechanism of bacterial motility. Nature. 1974 May 3;249(452):73–74. doi: 10.1038/249073a0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Slocum M. K., Parkinson J. S. Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: organization of the tar region. J Bacteriol. 1983 Aug;155(2):565–577. doi: 10.1128/jb.155.2.565-577.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Springer M. S., Goy M. F., Adler J. Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3312–3316. doi: 10.1073/pnas.74.8.3312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Springer W. R., Koshland D. E., Jr Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc Natl Acad Sci U S A. 1977 Feb;74(2):533–537. doi: 10.1073/pnas.74.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Spudich J. L., Koshland D. E., Jr Quantitation of the sensory response in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1975 Feb;72(2):710–713. doi: 10.1073/pnas.72.2.710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stock J. B., Koshland D. E., Jr A protein methylesterase involved in bacterial sensing. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3659–3663. doi: 10.1073/pnas.75.8.3659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Van Der Werf P., Koshland D. E., Jr Identification of a gamma-glutamyl methyl ester in bacterial membrane protein involved in chemotaxis. J Biol Chem. 1977 Apr 25;252(8):2793–2795. [PubMed] [Google Scholar]
  33. Wang E. A., Koshland D. E., Jr Receptor structure in the bacterial sensing system. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7157–7161. doi: 10.1073/pnas.77.12.7157. [DOI] [PMC free article] [PubMed] [Google Scholar]

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