An electrostatic mechanism closely reproducing observed behavior in the bacterial flagellar motor

Biophysical Journal

Volumn 78, Issue 2, 2000, Pages 626-651

  Walz, Dieter ^a   Caplan, S Roy ^b,c  

^a UNIVERSITY OF BASEL   (Switzerland)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACILLUS SUBTILIS; BIOMECHANICS; CONTROLLED STUDY; ESCHERICHIA COLI; FLAGELLUM; MOLECULAR DYNAMICS; MOTION; NONHUMAN; PH; PROTON TRANSPORT; STOICHIOMETRY; STREPTOCOCCUS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; STREPTOCOCCUS;

EID: 0034036511     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76622-7     Document Type: Article

References (65)

1. Alon, U., L. Camarena, M. G. Surette, B. Aguera y Areas, Y. Liu, S. Leibler, and J. B. Stock. 1998. Response regulator output in bacterial chemotaxis. EMBO J. 17:4238-4248.
2. Baldwin, J. M., R. Henderson, E. Beckman, and F. Zemlin. 1988. Images of purple membrane at 2.8 Å resolution obtained by cryo-electron microscopy. J. Mot. Biol. 202:585-591.
3. Berg, H. C., and S. Khan. 1983. A model for the flagellar rotary motor. In Mobility and Recognition in Cell Biology. H. Sund and C. Veeger, editors. DeGruyter, Berlin. 485-497.
4. Berg, H. C., and L. Turner. 1993. Torque generated by the flagellar motor of Escherichia coli. Biophys. J. 65:2201-2216.
5. Berry, R. M. 1993. Torque and switching in the bacterial flagellar motor. An electrostatic model. Biophys. J. 64:961-973.
6. Berry, R. M., and H. C. Berg. 1996. Torque generation by the bacterial flagellar motor close to stall. Biophys. J. 71:3501-3510.
7. Berry, R. M., and H. C. Berg. 1997. Absence of a barrier to backward rotation of the bacterial flagellar motor demonstrated with optical tweezers. Proc. Natl. Acad. Sci. USA. 94:14433-14437.
8. Berry, R. M., and H. C. Berg. 1999. Torque generation by the flagellar motor of Escherichia coli while driven backward. Biophys. J. 76: 580-587.
9. Berry, R. M., L. Turner, and H. C. Berg. 1995. Mechanical limits of bacterial flagellar motors probed by electrorotation. Biophys. J. 69: 280-286.
10. Blair, D. F., and H. C. Berg. 1988. Restoration of torque in defective flagellar motors. Science. 242:1678-1681.
11. Block, S. M., and H. C. Berg. 1984. Successive incorporation of force-generating units in the bacterial rotary motor. Nature (Lond.). 309: 470-472.
12. Braun, T. F., S. Poulson, J. B. Gully, J. C. Empey, S. van Way, A. Putnam, and D. F. Blair. 1999. Function of proline residues of MotA in torque generation by the flagellar motor of Escherichia coli. J. Bacteriol. 181:3542-3551.
13. Caplan, S. R. 1971. Nonequilibrium thermodynamics and its application to bioenergetics. In Current Topics in Bioenergetics. vol. 4, D. R. Sanadi, editor. Academic Press, New York. 1-79.
14. Caplan, S. R., and M. Kara-Ivanov. 1993. The bacterial flagellar motor. Intern. Rev. Cytol. 147:97-164.
15. Doering, C., B. Ermentrout, and G. Oster. 1995. Rotary DNA motors. Biophys. J. 69:2256-2267.
16. Eisenbach, M. 1996. Control of bacterial chemotaxis. Mol. Microbiol. 20:903-910.
17. Eisenbach, M., and S. R. Caplan. 1998. Bacterial chemotaxis: unsolved mystery of the flagellar switch. Curr. Biol. 8:R444-R446.
18. Elston, T. C., and G. Oster. 1997. Protein turbines I: the bacterial flagellar motor. Biophys. J. 73:703-721.
19. Felle, H., J. S. Porter, C. L. Slayman, and H. R. Kaback. 1980. Quantitative measurements of membrane potential in Escherichia coli. Biochemistry. 19:3585-3590.
20. Francis, N. R., G. E. Sosinsky, D. Thomas, and D. J. DeRosier. 1994. Isolation, characterization and structure of bacterial flagellar motors containing the switch complex. J. Mol. Biol. 235:1261-1270.
21. Fung, D. C., and H. C. Berg. 1995. Powering the flagellar motor of Escherichia coli with an external voltage source. Nature (Lond.). 375: 809-812.
22. Glasstone, S., K. J. Laidler, and H. Eyring. 1941. The Theory of Rate Processes. McGraw-Hill, New York.
23. Harvey, S. C. 1989. Treatment of electrostatic effects in macromolecular modeling. Proteins. 5:78-92.
24. Hill, T. L. 1977. Free Energy Transduction in Biology. Academic Press, New York.
25. Hirota, N., S. Matsuura, N. Mochizuki, N. Mutoh, and Y. Imae. 1981. Use of lipophilic cation-permeable mutants for measurement of transmembrane electrical potential in metabolizing cells of Escherichia coli. J. Bacteriol. 148:399-405.
26. Iwazawa, J., Y. Imae, and S. Kobayasi. 1993. Study of the torque of the bacterial flagellar motor using a rotating electric field. Biophys. J. 64:925-933.
27. Kami-ike, N., S. Kudo, and H. Hotani. 1991. Rapid changes in flagellar rotation induced by external electric pulses. Biophys. J. 60:1350-1355.
28. Kara-Ivanov, M., M. Eisenbach, and S. R. Caplan. 1995. Fluctuations in rotation rate of the flagellar motor of Escherichia coli. Biophys. J. 69:250-263.
29. +-ATPase of growing and resting, aerobic Escherichia coli. Biochemistry. 21:5534-5538.
30. Kedem, O., and S. R. Caplan. 1965. Degree of coupling and its relation to efficiency of energy conversion. Trans. Faraday Soc. 61:1897-1911.
31. Khan, S., M. Dapice, and I. Humayun. 1990. Energy transduction in the bacterial flagellar motor. Effects of load and pH. Biophys. J. 57: 779-796.
32. Khan, S., M. Dapice, and T. S. Reese. 1988. Effects of mot gene expression on the structure of the flagellar motor. J. Mol. Biol. 202:575-584.
33. Khan, S., D. Mack Key, and T. A. Krulwich. 1992. Membrane ultrastructure of alkaliphilic Bacillus species studied by rapid-freeze electron microscopy. J. Bacteriol. 174:5123-5126.
34. Kihara, M., M. Homma, K. Kutsukake, and R. M. Macnab. 1989. Flagellar switch of Salmonella typhimurium: gene sequence and deduced protein sequences. J. Bacteriol. 171:3247-3257.
35. Lapidus, I. R., M. Welch, and M. Eisenbach. 1988. Pausing of flagellar rotation is a component of bacterial motility and chemotaxis. J. Bacteriol. 170:3627-3631.
36. Lauger, P. 1977. Ion transport and rotation of bacterial flagella. Nature (Lond.). 268:360-362.
37. Lauger, P. 1988. Torque and rotation rate of the bacterial flagellar motor. Biophys. J. 53:53-65.
38. Lloyd, S. A., and D. F. Blair. 1997. Charged residues of the rotor protein FliG essential for torque generation in the flagellar motor of Escherichia coli. J. Mol. Biol. 266:733-744.
39. Lloyd, S. A., F. G. Whitby, D. F. Blair, and C. P. Hill. 1999. Structure of the C-terminal domain of FliG, a component of the rotor in the bacterial flagellar motor. Nature (Lond.). 400:472-475.
40. Lowe, G., M. Meister, and H. C. Berg. 1987. Rapid rotation of flagellar bundles in swimming bacteria. Nature (Lond.). 235:637-640.
41. Macnab, R. M. 1979. How do flagella propel bacteria? Trends Biochem. Sci. 4:N10-N13.
42. Macnab, R. M. 1995. Flagellar switch. In Two-Component Signal Transduction. J. A. Hoch and T. J. Silhavy, editors. American Society for Microbiology, Washington, DC. 181-199.
43. Macnab, R. M. 1996. Flagella and motility. In Escherichia coli and Salmonella: Cellular and Molecular Biology. F. C. Neidhardt, R. Curtiss, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger, editors. American Society far Microbiology, Washington, DC. 123-145.
44. McIntosh, J. E. A., and R. P. McIntosh. 1980. Mathematical Modeling and Computers in Endocrinology. Springer-Verlag, Berlin. 250-260.
45. Meister, M., S. R. Caplan, and H. C. Berg. 1989. Dynamics of a tightly coupled mechanism for flagellar rotation. Biophys. J. 55:905-914.
46. Meister, M., G. Lowe, and H. C. Berg. 1987. The proton flux through the bacterial flagellar motor. Cell. 49:643-650.
47. Samuel, A. D. T., and H. C. Berg. 1995. Fluctuation analysis of rotational speed of the bacterial flagellar motor. Proc. Natl. Acad. Sci. USA. 92:3502-3506.
48. Samuel, A. D. T., and H. C. Berg. 1996. Torque-generating units of the bacterial flagellar motor step independently. Biophys. J. 71:918-923.
49. Schuster, C. S., and S. Khan. 1994. The bacterial flagellar motor. Annu. Rev. Biophys. Biomol. Struct. 23:509-539.
50. Sharp, K. A., and B. Honig. 1990. Electrostatic interactions in macromolecules: theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19:301-332.
51. Sharp, L. L., J. Zhou, and D. F. Blair. 1995. Features of MotA proton channel structure revealed by tryptophan-scanning mutagenesis. Proc. Natl. Acad. Sci. USA. 92:7946-7950.
52. Shioi, J.-i., R. J. Galloway, M. Niwano, R. E. Chinnock, and B. L. Taylor. 1982. Requirement of ATP in bacterial chemotaxis. J. Biol. Chem. 257:7969-7975.
53. Shioi, J.-i., S. Matsuura, and Y. Imae. 1980. Quantitative measurements of proton motive force and motility in Bacillus subtilis. J. Bacteriol. 144:891-897.
54. Shioi, J., and B. L. Taylor. 1984. Oxygen taxis and proton motive force in Salmonella typhimurium. J. Biol. Chem. 259:10983-10988.
55. Sosinsky, G. E., N. R. Francis, M. J. B. Stallmeyer, and D. J. DeRosier. 1992. Substructure of the flagellar basal body of Salmonella typhimurium. J. Mol. biol. 223:171-184.
56. Turner, L., S. R. Caplan, and H. C. Berg. 1996. Temperature-induced switching of the bacterial flagellar motor. Biophys. J. 71:2227-2233.
57. 13DK106YW. Biophys. J. 77:597-603.
58. Voet. D., and J. G. Voet. 1995. Biochemistry. John Wiley, New York. 349.
59. Walz, D., and S. R. Caplan. 1988. Energy coupling and thermokinetic balancing in enzyme kinetics: microscopic reversibility and detailed balance revisited. Cell Biophys. 12:13-28.
60. Walz, D., and S. R. Caplan. 1995. Nonequilibrium thermodynamics and kinetics. In Bioelectrochemistry: Principles and Practice, Vol. 1, Bioelectrochemistry: General Introduction. S. R. Caplan, I. R. Miller, and G. Milazzo, editors. Birkhäuser, Basel, Switzerland. 1-48.
61. Walz, D., S. R. Caplan, D. R. L. Scriven, and D. C. Mikulecky. 1995a. Methods of mathematical modelling. In Bioelectrochemistry: Principles and Practice. Vol. 1, Bioelectrochemistry: General Introduction. S. R. Caplan, I. R. Miller, and G. Milazzo, editors. Birkhäuser, Basel, Switzerland. 49-131.
62. Walz, T., D. Typke, B. L. Smith, P. Agre, and A. Engel. 1995b. Projection map of aquaporin-1 determined by electron crystallography. Nature Struct. Biol. 2:730-732.
63. Washizu, M., Y. Kurahashi, H. Iochi, O. Kurosawa, S.-I. Aizawa, S. Kudo, Y. Magariyama, and H. Hotani. 1993. Dielectrophoretic measurement of bacterial motor characteristics. IEEE Trans. Ind. Applic. 29:286-294.
64. Zhao, R., C. D. Amsler, P. Matsumura, and S. Khan. 1996. FliG and FliM distribution in the Salmonella typhimurium cell and flagellar basal bodies. J. Bacteriol. 178:258-265.
65. Zhou, J., S. A. Lloyd, and D. F. Blair. 1998. Electrostatic interactions between rotor and stator in the bacterial flagellar motor. Proc. Natl. Acad Sci. USA. 95:6436-6441.