Abstract
The behavioral responses of chemotactic bacteria to environmental stimuli are initiated by a family of membrane-bound transducer proteins that communicate excitatory signals to the flagellar apparatus. The adaptation process appears to turn off the excitatory signal and is mediated by the reversible methylation of multiple sites on the transducer proteins. The activities of two chemotaxis-specific enzymes, a methyltransferase and a methylesterase, are regulated during adaptation to maintain behavioral responsiveness. To monitor stimulus-induced changes in methylesterase activity in intact cells, we quantitated the continuous generation of methanol, the end product of the demethylation reaction, in a flow device. In this paper we describe studies of the regulation of the demethylation process. Changes in methylesterase activity after the simultaneous addition of opposing stimuli through two different transducer classes suggest that the sensory information detected by these transducers was integrated and that this integrated signal controlled demethylation.
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Selected References
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- Adler J. Chemoreceptors in bacteria. Science. 1969 Dec 26;166(3913):1588–1597. doi: 10.1126/science.166.3913.1588. [DOI] [PubMed] [Google Scholar]
- 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]
- Berg H. C., Brown D. A. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature. 1972 Oct 27;239(5374):500–504. doi: 10.1038/239500a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Boyd A., Simon M. I. Multiple electrophoretic forms of methyl-accepting chemotaxis proteins generated by stimulus-elicited methylation in Escherichia coli. J Bacteriol. 1980 Aug;143(2):809–815. doi: 10.1128/jb.143.2.809-815.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chelsky D., Dahlquist F. W. Methyl-accepting chemotaxis proteins of Escherichia coli: methylated at three sites in a single tryptic fragment. Biochemistry. 1981 Feb 17;20(4):977–982. doi: 10.1021/bi00507a051. [DOI] [PubMed] [Google Scholar]
- Chelsky D., Dahlquist F. W. Structural studies of methyl-accepting chemotaxis proteins of Escherichia coli: evidence for multiple methylation sites. Proc Natl Acad Sci U S A. 1980 May;77(5):2434–2438. doi: 10.1073/pnas.77.5.2434. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chelsky D., Gutterson N. I., Koshland D. E., Jr A diffusion assay for detection and quantitation of methyl-esterified proteins on polyacrylamide gels. Anal Biochem. 1984 Aug 15;141(1):143–148. doi: 10.1016/0003-2697(84)90437-8. [DOI] [PubMed] [Google Scholar]
- Clarke S., Koshland D. E., Jr Membrane receptors for aspartate and serine in bacterial chemotaxis. J Biol Chem. 1979 Oct 10;254(19):9695–9702. [PubMed] [Google Scholar]
- DeFranco A. L., Koshland D. E., Jr Multiple methylation in processing of sensory signals during bacterial chemotaxis. Proc Natl Acad Sci U S A. 1980 May;77(5):2429–2433. doi: 10.1073/pnas.77.5.2429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeFranco A. L., Parkinson J. S., Koshland D. E., Jr Functional homology of chemotaxis genes in Escherichia coli and Salmonella typhimurium. J Bacteriol. 1979 Jul;139(1):107–114. doi: 10.1128/jb.139.1.107-114.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engström P., Hazelbauer G. L. Multiple methylation of methyl-accepting chemotaxis proteins during adaptation of E. coli to chemical stimuli. Cell. 1980 May;20(1):165–171. doi: 10.1016/0092-8674(80)90244-5. [DOI] [PubMed] [Google Scholar]
- Goldbeter A., Koshland D. E., Jr Simple molecular model for sensing and adaptation based on receptor modification with application to bacterial chemotaxis. J Mol Biol. 1982 Nov 5;161(3):395–416. doi: 10.1016/0022-2836(82)90246-7. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Hazelbauer G. L., Engström P., Harayama S. Methyl-accepting chemotaxis protein III and transducer gene trg. J Bacteriol. 1981 Jan;145(1):43–49. doi: 10.1128/jb.145.1.43-49.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Kehry M. R., Dahlquist F. W. Adaptation in bacterial chemotaxis: CheB-dependent modification permits additional methylations of sensory transducer proteins. Cell. 1982 Jul;29(3):761–772. doi: 10.1016/0092-8674(82)90438-x. [DOI] [PubMed] [Google Scholar]
- Kehry M. R., Dahlquist F. W. The methyl-accepting chemotaxis proteins of Escherichia coli. Identification of the multiple methylation sites on methyl-accepting chemotaxis protein I. J Biol Chem. 1982 Sep 10;257(17):10378–10386. [PubMed] [Google Scholar]
- Kehry M. R., Doak T. G., Dahlquist F. W. Aberrant regulation of methylesterase activity in cheD chemotaxis mutants of Escherichia coli. J Bacteriol. 1985 Jan;161(1):105–112. doi: 10.1128/jb.161.1.105-112.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kehry M. R., Doak T. G., Dahlquist F. W. Stimulus-induced changes in methylesterase activity during chemotaxis in Escherichia coli. J Biol Chem. 1984 Oct 10;259(19):11828–11835. [PubMed] [Google Scholar]
- Kihara M., Macnab R. M. Cytoplasmic pH mediates pH taxis and weak-acid repellent taxis of bacteria. J Bacteriol. 1981 Mar;145(3):1209–1221. doi: 10.1128/jb.145.3.1209-1221.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Kondoh H., Ball C. B., Adler J. Identification of a methyl-accepting chemotaxis protein for the ribose and galactose chemoreceptors of Escherichia coli. Proc Natl Acad Sci U S A. 1979 Jan;76(1):260–264. doi: 10.1073/pnas.76.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Parkinson J. S. Novel mutations affecting a signaling component for chemotaxis of Escherichia coli. J Bacteriol. 1980 Jun;142(3):953–961. doi: 10.1128/jb.142.3.953-961.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parkinson J. S., Parker S. R., Talbert P. B., Houts S. E. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J Bacteriol. 1983 Jul;155(1):265–274. doi: 10.1128/jb.155.1.265-274.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Reader R. W., Tso W. W., Springer M. S., Goy M. F., Adler J. Pleiotropic aspartate taxis and serine taxis mutants of Escherichia coli. J Gen Microbiol. 1979 Apr;111(2):363–374. doi: 10.1099/00221287-111-2-363. [DOI] [PubMed] [Google Scholar]
- Repaske D. R., Adler J. Change in intracellular pH of Escherichia coli mediates the chemotactic response to certain attractants and repellents. J Bacteriol. 1981 Mar;145(3):1196–1208. doi: 10.1128/jb.145.3.1196-1208.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ridgway H. G., Silverman M., Simon M. I. Localization of proteins controlling motility and chemotaxis in Escherichia coli. J Bacteriol. 1977 Nov;132(2):657–665. doi: 10.1128/jb.132.2.657-665.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- Stock J. B., Koshland D. E., Jr Changing reactivity of receptor carboxyl groups during bacterial sensing. J Biol Chem. 1981 Nov 10;256(21):10826–10833. [PubMed] [Google Scholar]
- Terwilliger T. C., Bogonez E., Wang E. A., Koshland D. E., Jr Sites of methyl esterification on the aspartate receptor involved in bacterial chemotaxis. J Biol Chem. 1983 Aug 25;258(16):9608–9611. [PubMed] [Google Scholar]
- 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]
- 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]
- Tso W. W., Adler J. Negative chemotaxis in Escherichia coli. J Bacteriol. 1974 May;118(2):560–576. doi: 10.1128/jb.118.2.560-576.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
