Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1996 Oct;71(4):2227–2233. doi: 10.1016/S0006-3495(96)79425-0

Temperature-induced switching of the bacterial flagellar motor.

L Turner 1, S R Caplan 1, H C Berg 1
PMCID: PMC1233691  PMID: 8889199

Abstract

Chemotaxis signaling proteins normally control the direction of rotation of the flagellar motor of Escherichia coli. In their absence, a wild-type motor spins exclusively counterclockwise. Although the signaling pathway is well defined, relatively little is known about switching, the mechanism that enables the motor to change direction. We found that switching occurs in the absence of signaling proteins when cells are cooled to temperatures below about 10 degrees C. The forward rate constant (for counterclockwise to clockwise, CCW to CW, switching) increases and the reverse rate constant (for CW to CCW switching) decreases as the temperature is lowered. At about -2 degrees C, most motors spin exclusively CW. At temperatures for which reversals are frequent enough to generate a sizable data set, both CCW and CW interval distributions appear to be exponential. From the rate constants we computed equilibrium constants and standard free energy changes, and from the temperature dependence of the standard free energy changes we determined standard enthalpy and entropy changes. Using transition-state theory, we also calculated the activation free energy, enthalpy, and entropy. We conclude that the CW state is preferred at very low temperatures and that it is relatively more highly bonded and restricted than the CCW state.

Full text

PDF
2230

Selected References

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

  1. Barak R., Eisenbach M. Regulation of interaction between signaling protein CheY and flagellar motor during bacterial chemotaxis. Curr Top Cell Regul. 1996;34:137–158. doi: 10.1016/s0070-2137(96)80005-7. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Berg H. C., Turner L. Torque generated by the flagellar motor of Escherichia coli. Biophys J. 1993 Nov;65(5):2201–2216. doi: 10.1016/S0006-3495(93)81278-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blair D. F. How bacteria sense and swim. Annu Rev Microbiol. 1995;49:489–522. doi: 10.1146/annurev.mi.49.100195.002421. [DOI] [PubMed] [Google Scholar]
  6. Block S. M., Segall J. E., Berg H. C. Adaptation kinetics in bacterial chemotaxis. J Bacteriol. 1983 Apr;154(1):312–323. doi: 10.1128/jb.154.1.312-323.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Block S. M., Segall J. E., Berg H. C. Impulse responses in bacterial chemotaxis. Cell. 1982 Nov;31(1):215–226. doi: 10.1016/0092-8674(82)90421-4. [DOI] [PubMed] [Google Scholar]
  8. Eisenbach M. Control of bacterial chemotaxis. Mol Microbiol. 1996 Jun;20(5):903–910. doi: 10.1111/j.1365-2958.1996.tb02531.x. [DOI] [PubMed] [Google Scholar]
  9. Hess J. F., Oosawa K., Kaplan N., Simon M. I. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell. 1988 Apr 8;53(1):79–87. doi: 10.1016/0092-8674(88)90489-8. [DOI] [PubMed] [Google Scholar]
  10. Hess J. F., Oosawa K., Matsumura P., Simon M. I. Protein phosphorylation is involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7609–7613. doi: 10.1073/pnas.84.21.7609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Khan S., Berg H. C. Isotope and thermal effects in chemiosmotic coupling to the flagellar motor of Streptococcus. Cell. 1983 Mar;32(3):913–919. doi: 10.1016/0092-8674(83)90076-4. [DOI] [PubMed] [Google Scholar]
  12. Khan S., Macnab R. M. The steady-state counterclockwise/clockwise ratio of bacterial flagellar motors is regulated by protonmotive force. J Mol Biol. 1980 Apr 15;138(3):563–597. doi: 10.1016/s0022-2836(80)80018-0. [DOI] [PubMed] [Google Scholar]
  13. Kuo S. C., Koshland D. E., Jr Multiple kinetic states for the flagellar motor switch. J Bacteriol. 1989 Nov;171(11):6279–6287. doi: 10.1128/jb.171.11.6279-6287.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. McLarnon J. G., Wang X. P. Temperature dependence of drug blockade of a calcium-dependent potassium channel in cultured hippocampal neurons. Biophys J. 1991 Nov;60(5):1278–1287. doi: 10.1016/S0006-3495(91)82161-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Oosawa K., Hess J. F., Simon M. I. Mutants defective in bacterial chemotaxis show modified protein phosphorylation. Cell. 1988 Apr 8;53(1):89–96. doi: 10.1016/0092-8674(88)90490-4. [DOI] [PubMed] [Google Scholar]
  17. Parkinson J. S. Behavioral genetics in bacteria. Annu Rev Genet. 1977;11:397–414. doi: 10.1146/annurev.ge.11.120177.002145. [DOI] [PubMed] [Google Scholar]
  18. Ravid S., Eisenbach M. Direction of flagellar rotation in bacterial cell envelopes. J Bacteriol. 1984 Apr;158(1):222–230. doi: 10.1128/jb.158.1.222-230.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shioi J. I., Galloway R. J., Niwano M., Chinnock R. E., Taylor B. L. Requirement of ATP in bacterial chemotaxis. J Biol Chem. 1982 Jul 25;257(14):7969–7975. [PubMed] [Google Scholar]
  20. 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]
  21. Stock A. M., Mowbray S. L. Bacterial chemotaxis: a field in motion. Curr Opin Struct Biol. 1995 Dec;5(6):744–751. doi: 10.1016/0959-440x(95)80006-9. [DOI] [PubMed] [Google Scholar]
  22. Wolfe A. J., Conley M. P., Kramer T. J., Berg H. C. Reconstitution of signaling in bacterial chemotaxis. J Bacteriol. 1987 May;169(5):1878–1885. doi: 10.1128/jb.169.5.1878-1885.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wylie D., Stock A., Wong C. Y., Stock J. Sensory transduction in bacterial chemotaxis involves phosphotransfer between Che proteins. Biochem Biophys Res Commun. 1988 Mar 15;151(2):891–896. doi: 10.1016/s0006-291x(88)80365-6. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES