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. 1997 May;179(10):3196–3201. doi: 10.1128/jb.179.10.3196-3201.1997

Glycerol elicits energy taxis of Escherichia coli and Salmonella typhimurium.

I B Zhulin 1, E H Rowsell 1, M S Johnson 1, B L Taylor 1
PMCID: PMC179097  PMID: 9150214

Abstract

Escherichia coli and Salmonella typhimurium show positive chemotaxis to glycerol, a chemical previously reported to be a repellent for E. coli. The threshold of the attractant response in both species was 10(-6) M glycerol. Glycerol chemotaxis was energy dependent and coincident with an increase in membrane potential. Metabolism of glycerol was required for chemotaxis, and when lactate was present to maintain energy production in the absence of glycerol, the increases in membrane potential and chemotactic response upon addition of glycerol were abolished. Methylation of a chemotaxis receptor was not required for positive glycerol chemotaxis in E. coli or S. typhimurium but is involved in the negative chemotaxis of E. coli to high concentrations of glycerol. We propose that positive chemotaxis to glycerol in E. coli and S. typhimurium is an example of energy taxis mediated via a signal transduction pathway that responds to changes in the cellular energy level.

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Selected References

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  1. Adler J. Chemoreceptors in bacteria. Science. 1969 Dec 26;166(3913):1588–1597. doi: 10.1126/science.166.3913.1588. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Aswad D., Koshland D. E., Jr Isolation, characterization and complementation of Salmonella typhimurium chemotaxis mutants. J Mol Biol. 1975 Sep 15;97(2):225–235. doi: 10.1016/s0022-2836(75)80036-2. [DOI] [PubMed] [Google Scholar]
  4. Aswad D., Koshland D. E., Jr Role of methionine in bacterial chemotaxis. J Bacteriol. 1974 May;118(2):640–645. doi: 10.1128/jb.118.2.640-645.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bespalov V. A., Zhulin I. B., Taylor B. L. Behavioral responses of Escherichia coli to changes in redox potential. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10084–10089. doi: 10.1073/pnas.93.19.10084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bourret R. B., Borkovich K. A., Simon M. I. Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu Rev Biochem. 1991;60:401–441. doi: 10.1146/annurev.bi.60.070191.002153. [DOI] [PubMed] [Google Scholar]
  7. Brass J. M., Manson M. D. Reconstitution of maltose chemotaxis in Escherichia coli by addition of maltose-binding protein to calcium-treated cells of maltose regulon mutants. J Bacteriol. 1984 Mar;157(3):881–890. doi: 10.1128/jb.157.3.881-890.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Budrene E. O., Berg H. C. Dynamics of formation of symmetrical patterns by chemotactic bacteria. Nature. 1995 Jul 6;376(6535):49–53. doi: 10.1038/376049a0. [DOI] [PubMed] [Google Scholar]
  9. Clancy M., Madill K. A., Wood J. M. Genetic and biochemical requirements for chemotaxis to L-proline in Escherichia coli. J Bacteriol. 1981 Jun;146(3):902–906. doi: 10.1128/jb.146.3.902-906.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Dang C. V., Niwano M., Ryu J., Taylor B. L. Inversion of aerotactic response in Escherichia coli deficient in cheB protein methylesterase. J Bacteriol. 1986 Apr;166(1):275–280. doi: 10.1128/jb.166.1.275-280.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Johnson M. S., Taylor B. L. Comparison of methods for specific depletion of ATP in Salmonella typhimurium. Appl Environ Microbiol. 1993 Oct;59(10):3509–3512. doi: 10.1128/aem.59.10.3509-3512.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Laszlo D. J., Taylor B. L. Aerotaxis in Salmonella typhimurium: role of electron transport. J Bacteriol. 1981 Feb;145(2):990–1001. doi: 10.1128/jb.145.2.990-1001.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Li C., Adler J. Escherichia coli shows two types of behavioral responses to osmotic upshift. J Bacteriol. 1993 May;175(9):2564–2567. doi: 10.1128/jb.175.9.2564-2567.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Li C., Boileau A. J., Kung C., Adler J. Osmotaxis in Escherichia coli. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9451–9455. doi: 10.1073/pnas.85.24.9451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lindbeck J. C., Goulbourne E. A., Jr, Johnson M. S., Taylor B. L. Aerotaxis in Halobacterium salinarium is methylation-dependent. Microbiology. 1995 Nov;141(Pt 11):2945–2953. doi: 10.1099/13500872-141-11-2945. [DOI] [PubMed] [Google Scholar]
  19. Lux R., Jahreis K., Bettenbrock K., Parkinson J. S., Lengeler J. W. Coupling the phosphotransferase system and the methyl-accepting chemotaxis protein-dependent chemotaxis signaling pathways of Escherichia coli. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11583–11587. doi: 10.1073/pnas.92.25.11583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Manson M. D. Bacterial motility and chemotaxis. Adv Microb Physiol. 1992;33:277–346. doi: 10.1016/s0065-2911(08)60219-2. [DOI] [PubMed] [Google Scholar]
  21. Manson M. D., Tedesco P., Berg H. C., Harold F. M., Van der Drift C. A protonmotive force drives bacterial flagella. Proc Natl Acad Sci U S A. 1977 Jul;74(7):3060–3064. doi: 10.1073/pnas.74.7.3060. [DOI] [PMC free article] [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. Oosawa K., Imae Y. Demethylation of methyl-accepting chemotaxis proteins in Escherichia coli induced by the repellents glycerol and ethylene glycol. J Bacteriol. 1984 Feb;157(2):576–581. doi: 10.1128/jb.157.2.576-581.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oosawa K., Imae Y. Glycerol and ethylene glycol: members of a new class of repellents of Escherichia coli chemotaxis. J Bacteriol. 1983 Apr;154(1):104–112. doi: 10.1128/jb.154.1.104-112.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Parkinson J. S. Signal transduction schemes of bacteria. Cell. 1993 Jun 4;73(5):857–871. doi: 10.1016/0092-8674(93)90267-t. [DOI] [PubMed] [Google Scholar]
  28. Rowsell E. H., Smith J. M., Wolfe A., Taylor B. L. CheA, CheW, and CheY are required for chemotaxis to oxygen and sugars of the phosphotransferase system in Escherichia coli. J Bacteriol. 1995 Oct;177(20):6011–6014. doi: 10.1128/jb.177.20.6011-6014.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shioi J., Dang C. V., Taylor B. L. Oxygen as attractant and repellent in bacterial chemotaxis. J Bacteriol. 1987 Jul;169(7):3118–3123. doi: 10.1128/jb.169.7.3118-3123.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shioi J., Taylor B. L. Oxygen taxis and proton motive force in Salmonella typhimurium. J Biol Chem. 1984 Sep 10;259(17):10983–10988. [PubMed] [Google Scholar]
  31. Shioi J., Tribhuwan R. C., Berg S. T., Taylor B. L. Signal transduction in chemotaxis to oxygen in Escherichia coli and Salmonella typhimurium. J Bacteriol. 1988 Dec;170(12):5507–5511. doi: 10.1128/jb.170.12.5507-5511.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. Taylor B. L., Miller J. B., Warrick H. M., Koshland D. E., Jr Electron acceptor taxis and blue light effect on bacterial chemotaxis. J Bacteriol. 1979 Nov;140(2):567–573. doi: 10.1128/jb.140.2.567-573.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Taylor B. L. Role of proton motive force in sensory transduction in bacteria. Annu Rev Microbiol. 1983;37:551–573. doi: 10.1146/annurev.mi.37.100183.003003. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Wolfe A. J., Berg H. C. Migration of bacteria in semisolid agar. Proc Natl Acad Sci U S A. 1989 Sep;86(18):6973–6977. doi: 10.1073/pnas.86.18.6973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wong L. S., Johnson M. S., Sandberg L. B., Taylor B. L. Amino acid efflux in response to chemotactic and osmotic signals in Bacillus subtilis. J Bacteriol. 1995 Aug;177(15):4342–4349. doi: 10.1128/jb.177.15.4342-4349.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yonekawa H., Hayashi H., Parkinson J. S. Requirement of the cheB function for sensory adaptation in Escherichia coli. J Bacteriol. 1983 Dec;156(3):1228–1235. doi: 10.1128/jb.156.3.1228-1235.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zhulin I. B., Bespalov V. A., Johnson M. S., Taylor B. L. Oxygen taxis and proton motive force in Azospirillum brasilense. J Bacteriol. 1996 Sep;178(17):5199–5204. doi: 10.1128/jb.178.17.5199-5204.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]

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