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. 1993 Apr;64(4):961–973. doi: 10.1016/S0006-3495(93)81462-0

Torque and switching in the bacterial flagellar motor. An electrostatic model.

R M Berry 1
PMCID: PMC1262414  PMID: 7684268

Abstract

A model is presented for the rotary motor that drives bacterial flagella, using the electrochemical gradient of protons across the cytoplasmic membrane. The model unifies several concepts present in previous models. Torque is generated by proton-conducting particles around the perimeter of the rotor at the base of the flagellum. Protons in channels formed by these particles interact electrostatically with tilted lines of charges on the rotor, providing "loose coupling" between proton flux and rotation of the flagellum. Computer simulations of the model correctly predict the experimentally observed dynamic properties of the motor. Unlike previous models, the motor presented here may rotate either way for a given direction of the protonmotive force. The direction of rotation only depends on the level of occupancy of the proton channels. This suggests a novel and simple mechanism for the switching between clockwise and counterclockwise rotation that is the basis of bacterial chemotaxis.

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Selected References

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

  1. Barak R., Eisenbach M. Correlation between phosphorylation of the chemotaxis protein CheY and its activity at the flagellar motor. Biochemistry. 1992 Feb 18;31(6):1821–1826. doi: 10.1021/bi00121a034. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Blair D. F., Berg H. C. The MotA protein of E. coli is a proton-conducting component of the flagellar motor. Cell. 1990 Feb 9;60(3):439–449. doi: 10.1016/0092-8674(90)90595-6. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Edmonds D. T. A kinetic role for ionizable sites in membrane channel proteins. Eur Biophys J. 1989;17(3):113–119. doi: 10.1007/BF00254764. [DOI] [PubMed] [Google Scholar]
  7. Eisenbach M., Wolf A., Welch M., Caplan S. R., Lapidus I. R., Macnab R. M., Aloni H., Asher O. Pausing, switching and speed fluctuation of the bacterial flagellar motor and their relation to motility and chemotaxis. J Mol Biol. 1990 Feb 5;211(3):551–563. doi: 10.1016/0022-2836(90)90265-N. [DOI] [PubMed] [Google Scholar]
  8. Glagolev A. N., Skulachev V. P. The proton pump is a molecular engine of motile bacteria. Nature. 1978 Mar 16;272(5650):280–282. doi: 10.1038/272280a0. [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. Hill T. L. Studies in irreversible thermodynamics. IV. Diagrammatic representation of steady state fluxes for unimolecular systems. J Theor Biol. 1966 Apr;10(3):442–459. doi: 10.1016/0022-5193(66)90137-8. [DOI] [PubMed] [Google Scholar]
  11. Hirota N., Imae Y. Na+-driven flagellar motors of an alkalophilic Bacillus strain YN-1. J Biol Chem. 1983 Sep 10;258(17):10577–10581. [PubMed] [Google Scholar]
  12. Jones C. J., Aizawa S. The bacterial flagellum and flagellar motor: structure, assembly and function. Adv Microb Physiol. 1991;32:109–172. doi: 10.1016/s0065-2911(08)60007-7. [DOI] [PubMed] [Google Scholar]
  13. Jones C. J., Homma M., Macnab R. M. L-, P-, and M-ring proteins of the flagellar basal body of Salmonella typhimurium: gene sequences and deduced protein sequences. J Bacteriol. 1989 Jul;171(7):3890–3900. doi: 10.1128/jb.171.7.3890-3900.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kami-ike N., Kudo S., Hotani H. Rapid changes in flagellar rotation induced by external electric pulses. Biophys J. 1991 Dec;60(6):1350–1355. doi: 10.1016/S0006-3495(91)82172-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kashket E. R. The proton motive force in bacteria: a critical assessment of methods. Annu Rev Microbiol. 1985;39:219–242. doi: 10.1146/annurev.mi.39.100185.001251. [DOI] [PubMed] [Google Scholar]
  16. Khan S., Dapice M., Humayun I. Energy transduction in the bacterial flagellar motor. Effects of load and pH. Biophys J. 1990 Apr;57(4):779–796. doi: 10.1016/S0006-3495(90)82598-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Khan S., Dapice M., Reese T. S. Effects of mot gene expression on the structure of the flagellar motor. J Mol Biol. 1988 Aug 5;202(3):575–584. doi: 10.1016/0022-2836(88)90287-2. [DOI] [PubMed] [Google Scholar]
  18. Khan S., Macnab R. M. Proton chemical potential, proton electrical potential and bacterial motility. J Mol Biol. 1980 Apr 15;138(3):599–614. doi: 10.1016/s0022-2836(80)80019-2. [DOI] [PubMed] [Google Scholar]
  19. Khan S., Meister M., Berg H. C. Constraints on flagellar rotation. J Mol Biol. 1985 Aug 20;184(4):645–656. doi: 10.1016/0022-2836(85)90310-9. [DOI] [PubMed] [Google Scholar]
  20. Kihara M., Homma M., Kutsukake K., Macnab R. M. Flagellar switch of Salmonella typhimurium: gene sequences and deduced protein sequences. J Bacteriol. 1989 Jun;171(6):3247–3257. doi: 10.1128/jb.171.6.3247-3257.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kudo S., Magariyama Y., Aizawa S. Abrupt changes in flagellar rotation observed by laser dark-field microscopy. Nature. 1990 Aug 16;346(6285):677–680. doi: 10.1038/346677a0. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. Meister M., Berg H. C. The stall torque of the bacterial flagellar motor. Biophys J. 1987 Sep;52(3):413–419. doi: 10.1016/S0006-3495(87)83230-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Murata T., Yano M., Shimizu H. A model for bacterial flagellar motor: free energy transduction and self-organization of rotational motion. J Theor Biol. 1989 Aug 22;139(4):531–559. doi: 10.1016/s0022-5193(89)80069-4. [DOI] [PubMed] [Google Scholar]
  29. Neumcke B., Läuger P. Nonlinear electrical effects in lipid bilayer membranes. II. Integration of the generalized Nernst-Planck equations. Biophys J. 1969 Sep;9(9):1160–1170. doi: 10.1016/S0006-3495(69)86443-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Prod'hom B., Pietrobon D., Hess P. Direct measurement of proton transfer rates to a group controlling the dihydropyridine-sensitive Ca2+ channel. Nature. 1987 Sep 17;329(6136):243–246. doi: 10.1038/329243a0. [DOI] [PubMed] [Google Scholar]
  32. Ravid S., Matsumura P., Eisenbach M. Restoration of flagellar clockwise rotation in bacterial envelopes by insertion of the chemotaxis protein CheY. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7157–7161. doi: 10.1073/pnas.83.19.7157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shimada K., Berg H. C. Response of the flagellar rotary motor to abrupt changes in extracellular pH. J Mol Biol. 1987 Feb 5;193(3):585–589. doi: 10.1016/0022-2836(87)90269-5. [DOI] [PubMed] [Google Scholar]
  34. Stallmeyer M. J., Aizawa S., Macnab R. M., DeRosier D. J. Image reconstruction of the flagellar basal body of Salmonella typhimurium. J Mol Biol. 1989 Feb 5;205(3):519–528. doi: 10.1016/0022-2836(89)90223-4. [DOI] [PubMed] [Google Scholar]
  35. Ueno T., Oosawa K., Aizawa S. M ring, S ring and proximal rod of the flagellar basal body of Salmonella typhimurium are composed of subunits of a single protein, FliF. J Mol Biol. 1992 Oct 5;227(3):672–677. doi: 10.1016/0022-2836(92)90216-7. [DOI] [PubMed] [Google Scholar]
  36. Wagenknecht T. A plausible mechanism for flagellar rotation in bacteria. FEBS Lett. 1986 Feb 17;196(2):193–197. doi: 10.1016/0014-5793(86)80244-7. [DOI] [PubMed] [Google Scholar]
  37. Yamaguchi S., Aizawa S., Kihara M., Isomura M., Jones C. J., Macnab R. M. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J Bacteriol. 1986 Dec;168(3):1172–1179. doi: 10.1128/jb.168.3.1172-1179.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

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