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. 1999 Jan;76(1 Pt 1):580–587. doi: 10.1016/S0006-3495(99)77226-7

Torque generated by the flagellar motor of Escherichia coli while driven backward.

R M Berry 1, H C Berg 1
PMCID: PMC1302548  PMID: 9876171

Abstract

The technique of electrorotation was used to apply torque to cells of the bacterium Escherichia coli tethered to glass coverslips by single flagella. Cells were made to rotate backward, that is, in the direction opposite to the rotation driven by the flagellar motor itself. The torque generated by the motor under these conditions was estimated using an analysis that explicitly considers the angular dependence of both the viscous drag coefficient of the cell and the torque produced by electrorotation. Motor torque varied approximately linearly with speed up to over 100 Hz in either direction, placing constraints on mechanisms for torque generation in which rates of proton transfer for backward rotation are limiting. These results, interpreted in the context of a simple three-state kinetic model, suggest that the rate-limiting step in the torque-generating cycle is a powerstroke in which motor rotation and dissipation of the energy available from proton transit occur synchronously.

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Selected References

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

  1. Berg H. C. Dynamic properties of bacterial flagellar motors. Nature. 1974 May 3;249(452):77–79. doi: 10.1038/249077a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Berry R. M., Berg H. C. Absence of a barrier to backwards rotation of the bacterial flagellar motor demonstrated with optical tweezers. Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14433–14437. doi: 10.1073/pnas.94.26.14433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berry R. M., Berg H. C. Torque generated by the bacterial flagellar motor close to stall. Biophys J. 1996 Dec;71(6):3501–3510. doi: 10.1016/S0006-3495(96)79545-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berry R. M. Torque and switching in the bacterial flagellar motor. An electrostatic model. Biophys J. 1993 Apr;64(4):961–973. doi: 10.1016/S0006-3495(93)81462-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blair D. F., Berg H. C. Restoration of torque in defective flagellar motors. Science. 1988 Dec 23;242(4886):1678–1681. doi: 10.1126/science.2849208. [DOI] [PubMed] [Google Scholar]
  7. Block S. M., Berg H. C. Successive incorporation of force-generating units in the bacterial rotary motor. 1984 May 31-Jun 6Nature. 309(5967):470–472. doi: 10.1038/309470a0. [DOI] [PubMed] [Google Scholar]
  8. Coppin C. M., Pierce D. W., Hsu L., Vale R. D. The load dependence of kinesin's mechanical cycle. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8539–8544. doi: 10.1073/pnas.94.16.8539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elston T. C., Oster G. Protein turbines. I: The bacterial flagellar motor. Biophys J. 1997 Aug;73(2):703–721. doi: 10.1016/S0006-3495(97)78104-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jones C. J., Macnab R. M., Okino H., Aizawa S. Stoichiometric analysis of the flagellar hook-(basal-body) complex of Salmonella typhimurium. J Mol Biol. 1990 Mar 20;212(2):377–387. doi: 10.1016/0022-2836(90)90132-6. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Läuger P. Torque and rotation rate of the bacterial flagellar motor. Biophys J. 1988 Jan;53(1):53–65. doi: 10.1016/S0006-3495(88)83065-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Magariyama Y., Sugiyama S., Muramoto K., Maekawa Y., Kawagishi I., Imae Y., Kudo S. Very fast flagellar rotation. Nature. 1994 Oct 27;371(6500):752–752. doi: 10.1038/371752b0. [DOI] [PubMed] [Google Scholar]
  15. Meister M., Caplan S. R., Berg H. C. Dynamics of a tightly coupled mechanism for flagellar rotation. Bacterial motility, chemiosmotic coupling, protonmotive force. Biophys J. 1989 May;55(5):905–914. doi: 10.1016/S0006-3495(89)82889-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Meister M., Lowe G., Berg H. C. The proton flux through the bacterial flagellar motor. Cell. 1987 Jun 5;49(5):643–650. doi: 10.1016/0092-8674(87)90540-x. [DOI] [PubMed] [Google Scholar]
  17. Oosawa F., Hayashi S. The loose coupling mechanism in molecular machines of living cells. Adv Biophys. 1986;22:151–183. doi: 10.1016/0065-227x(86)90005-5. [DOI] [PubMed] [Google Scholar]
  18. Samuel A. D., Berg H. C. Fluctuation analysis of rotational speeds of the bacterial flagellar motor. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3502–3506. doi: 10.1073/pnas.92.8.3502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Samuel A. D., Berg H. C. Torque-generating units of the bacterial flagellar motor step independently. Biophys J. 1996 Aug;71(2):918–923. doi: 10.1016/S0006-3495(96)79295-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Scharf B. E., Fahrner K. A., Turner L., Berg H. C. Control of direction of flagellar rotation in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):201–206. doi: 10.1073/pnas.95.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Sosinsky G. E., Francis N. R., DeRosier D. J., Wall J. S., Simon M. N., Hainfeld J. Mass determination and estimation of subunit stoichiometry of the bacterial hook-basal body flagellar complex of Salmonella typhimurium by scanning transmission electron microscopy. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4801–4805. doi: 10.1073/pnas.89.11.4801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zhou J., Lloyd S. A., Blair D. F. Electrostatic interactions between rotor and stator in the bacterial flagellar motor. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6436–6441. doi: 10.1073/pnas.95.11.6436. [DOI] [PMC free article] [PubMed] [Google Scholar]

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