Constraints on models for the flagellar rotary motor

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 355, Issue 1396, 2000, Pages 491-501

  Berg, Howard C ^a,b,c  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bacteria; Escherichia coli; Flagellum; Motility; Rotary motor

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA TYPHIMURIUM; TYPHIMURIUM;

EID: 0034728850     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2000.0590     Document Type: Conference Paper

References (128)

1. Aizawa, S.-I. 1996 Flagellar assembly in Salmonella typhimurium. Mol. Microbiol. 19, 1-5.
2. +-driven flagellar motors of alkalophilic Bacillus strains by the amiloride analog phenamil. J. Bacteriol. 172, 1634-1639.
3. + ions as a direct source of energy during bacterial locomotion. Biochemistry 41, 1206-1210.
4. Berg, H. C. 1974 Dynamic properties of bacterial flagellar motors. Nature 249, 77-79.
5. Berg, H. C. 1976 Does the flagellar rotary motor step? In Cell motility, Cold Spring Harbor conferences on cell proliferation, vol. 3 (ed. R. Goldman, T. Pollard & J. Rosenbaum), pp. 47-56. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
6. Berg, H. C. 1996 Symmetries in bacterial motility. Proc. Natl Acad. Sci. USA 93, 14 225-14 228.
7. Berg, H. C. & Anderson, R. A. 1973 Bacteria swim by rotating their flagellar filaments. Nature 245, 380-382.
8. Berg, H. C. & Khan, S. 1983 A model for the flagellar rotary motor. In Mobility and recognition in cell biology (ed. H. Sund & C. Veeger), pp. 485-497. Berlin: deGruyter.
9. Berg, H. C. & Turner, L. 1979 Movement of microorganisms in viscous environments. Nature 278, 349-351.
10. Berg, H. C. & Turner, L. 1993 Torque generated by the flagellar motor of Escherichia coli. Biophys. J. 65, 2201-2216.
11. Berg, H. C., Manson, M. D. & Conley, M. P. 1982 Dynamics and energetics of flagellar rotation in bacteria. Symp. Soc. Exp. Biol. 35, 1-31.
12. Berry, R. M. & Berg, H. C. 1996 Torque generated by the bacterial flagellar motor close to stall. Biophys. J. 71, 3501-3510.
13. Berry, R. M. & Berg, H. C. 1997 Absence of a barrier to backwards rotation of the bacterial flagellar motor demonstrated with optical tweezers. Proc. Natl Acad. Sci. USA 94, 14 433-14 437.
14. Berry, R. M. & Berg, H. C. 1999 Torque generated by the flagellar motor of Escherichia coli while driven backwards. Biophys. J. 76, 580-587.
15. Blair, D. F. & Berg, H. C. 1988 Restoration of torque in defective flagellar motors. Science 242, 1678-1681.
16. Blair, D. F. & Berg, H. C. 1990 The MotA protein of Escherichia coli is a proton-conducting component of the flagellar motor. Cell 60, 439-449.
17. Blair, D. F. & Berg, H. C. 1991 Mutants in the MotA protein of Escherichia coli reveal domains critical for proton conduction. J. Mol. Biol. 221, 1433-1442.
18. Block, S. M. & Berg, H. C. 1984 Successive incorporation of force-generating units in the bacterial rotary motor. Nature 309, 470-472.
19. Braun, T. F., Poulson, S., Gully, J. B., Empey, J. C., Van Way, S., Putnam, A. & Blair, D. F. 1999 Function of proline residues of MotA in torque generation by the flagellar motor of Escherichia coli. J. Bacteriol. 181, 3542-3551.
20. Caplan, S. R. & Kara-Ivanov, M. 1993 The bacterial flagellar motor. Int. Rev. Cytol. 147, 97-164.
21. Chen, X. & Berg, H. C. 2000 Torque-speed relationships of the flagellar rotary motor of Escherichia coli. Biophys. J. 78, 1036-1041.
22. Chun, S. Y. & Parkinson, J. S. 1988 Bacterial motility: membrane topology of the Escherichia coli MotB protein. Science 239, 276-278.
23. Conley, M. P. & Berg, H. C. 1984 Chemical modification of Streptococcus flagellar motors. J. Bacteriol. 158, 832-843.
24. Coulton, J. W. & Murray, R. G. E. 1978 Cell envelope associations of Aquaspirillum serpens flagella. J. Bacteriol. 136, 1047-1049.
25. Cox, D. R. & Lewis, P. A. W. 1966 The statistical analysis of series of events. London: Methuen.
26. Dailey, F. E. & Berg, H. C. 1993 Mutants in disulfide bond formation that disrupt flagellar assembly. Proc. Natl Acad. Sci. USA 90, 1043-1047.
27. Dean, G. E., Macnab, R. M., Stader, J., Matsumura, P. & Burke, C. 1984 Gene sequence and predicted amino acid sequence of the MotA protein, a membrane-associated protein required for flagellar rotation in Escherichia coli. J. Bacteriol. 159, 991-999.
28. De Mot, R. & Vanderleyden, J. 1994 The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both Gram-positive and Gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan. Mol. Microbiol. 12, 333-334.
29. DePamphilis, M. L. & Adler, J. 1971a Fine structure and isolation of the hook basal body complex of flagella from Escherichia coli and Bacillus subtilis. J. Bacteriol. 105, 384-395.
30. DePamphilis, M. L. & Adler, J. 1971b Attachment of flagellar basal bodies to the cell envelope: specific attachment to the outer, lipopolysaccharide membrane and the cytoplasmic membrane. J. Bacteriol. 105, 396-407.
31. Driks, A. & DeRosier, D. J. 1990 Additional structures associated with bacterial flagellar basal body. J. Mol. Biol. 211, 669-672.
32. Elston, T. C. & Oster, G. 1997 Protein turbines. I. The bacterial flagellar motor. Biophys. J. 73, 703-721.
33. Emerson, S. U., Tokuyasu, K. & Simon, M. I. 1970 Bacterial flagella: polarity of elongation. Science 169, 190-192.
34. Fan, F., Ohnishi, K., Francis, N. R. & Macnab, R. M. 1997 The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body. Mol. Microbiol. 26, 1035-1046.
35. Francis, N. R., Irikura, V. M., Yamaguchi, S., DeRosier, D. J. & Macnab, R. M. 1992 Localization of the Salmonella typhimurium flagellar switch protein FliG to the cytoplasmic M-ring face of the basal body. Proc. Natl Acad. Sci. USA 89, 6304-6308.
36. Francis, N. R., Sosinsky, G. E., Thomas, D. & DeRosier, D. J. 1994 Isolation, characterization and structure of bacterial flagellar motors containing the switch complex. J. Mol. Biol. 235, 1261-1270.
37. Fung, D. C. & Berg, H. C. 1995 Powering the flagellar motor of Escherichia coli with an external voltage source. Nature 375, 809-812.
38. Garcia de la Torre, J. & Bloomfield, V. A. 1981 Hydrodynamic properties of complex, rigid, biological macromolecules: theory and applications. Q. Rev. Biophys. 14, 81-139.
39. Glagolev, A. N. & Skulachev, V. P. 1978 The proton pump is a molecular engine of motile bacteria. Nature 272, 280-282.
40. Harold, F. M. & Maloney, P. C. 1996 Energy transduction by ion currents. In Escherichia coli and Salmonella: cellular and molecular biology, vol. 1 (ed. F. C. Neidhardt, R. Curtiss, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter & H. E. Umbarger), pp. 283-306. Washington, DC: American Society for Microbiology.
41. Hirano, T., Yamaguchi, S., Oosawa, K. & Aizawa, S.-I. 1994 Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J. Bacteriol. 176, 5439-5449.
42. Homma, M., Fujita, H., Yamaguchi, S. & Iino, T. 1984 Excretion of unassembled flagellin by Salmonella typhimurium mutants deficient in hook-associated proteins. J. Bacteriol. 159, 1056-1059.
43. Homma, M., Komeda, Y., Iino, T. & Macnab, R. M. 1987 The flaFIX gene product of Salmonella typhimurium is a flagellar basal body component with a signal peptide for export. J. Bacteriol. 169, 1493-1498.
44. Iino, T. 1969 Polarity of flagellar growth in Salmonella. J. Gen. Microbiol. 56, 227-239.
45. Iino, T. 1974 Assembly of Salmonella flagellin in vitro and in vivo. J. Supramol. Struct. 2, 372-384.
46. Iino, T., Komeda, Y., Kutsukake, K., Macnab, R. M., Matsumura, P., Parkinson. J. S., Simon, M. I. & Yamaguchi, S. 1988 New unified nomenclature for the flagellar genes of Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 52, 533-535.
47. Ikeda, T., Homma, M., Iino, T, Asakura, S. & Kamiya, R. 1987 Localization and stoichiometry of hook-associated proteins within Salmonella typhimurium flagella. J. Bacteriol. 169, 1168-1173.
48. Ikeda, T., Yamaguchi, S. & Hotani, H. 1993 Flagellar growth in a filament-less Salmonella fliD mutant supplemented with purified hook-associated protein 2. J. Biochem. 114, 39-44.
49. Ikeda, T., Oosawa, K. & Hotani, H. 1996 Self-assembly of the filament capping protein, FliD, of bacterial flagella into an annular structure. J. Mol. Biol. 259, 679-686.
50. + in energy transduction. In New era of bioenergetics (ed. Y. Mukohata), pp. 197-221. Tokyo: Academic Press.
51. +-driven bacterial flagellar motors. J. Bioenerg. Biomembr. 21, 705-716.
52. Iwazawa, J., Imae, Y. & Kobayasi, S. 1993 Study of the torque of the bacterial flagellar motor using a rotating electric field. Biophys. J. 64, 925-933.
53. Jeffery, G. B. 1915 On the steady rotation of a solid of revolution in a viscous fluid. Proc. Lond. Math. Soc. 14, 327-338.
54. Jones, C. J., Homma, M. & Macnab, R. M. 1989 L-, P-, and M-ring proteins of the flagellar basal body of Salmonella typhimurium: gene sequences and deduced protein sequences. J. Bacteriol. 171, 3890-3900.
55. Kagawa, H., Morisawa, H. & Enomoto, M. 1981 Reconstitution in vitro of flagellar filaments onto hook structures attached to bacterial cells. J. Mol. Biol. 153, 465-470.
56. Kagawa, H., Nishiyama, T. & Yamaguchi, S. 1983 Motility development of Salmonella typhimurium cells with flaV mutations after addition of exogenous flagellin. J. Bacteriol. 155, 435-437.
57. Kami-ike, N., Kudo, S. & Hotani, H. 1991 Rapid changes in flagellar rotation induced by external electric pulses. Biophys. J. 60, 1350-1355.
58. Kara-Ivanov, M., Eisenbach, M. & Caplan, S. R. 1995 Fluctuations in rotation rate of the flagellar motor of Escherichia coli. Biophys. J. 69, 250-263.
59. Kashket, E. R. 1985 The proton motive force in bacteria: a critical assessment of methods. A. Rev. Microbiol. 39, 219-242.
60. Khan, I. H., Reese, T. S. & Khan, S. 1992 The cytoplasmic component of the bacterial flagellar motor. Proc. Natl Acad. Sci. USA 89, 5956-5960.
61. Khan, S. & Berg, H. C. 1983 Isotope and thermal effects in chemiosmotic coupling to the flagellar motor of Streptococcus. Cell 32, 913-919.
62. Khan, S. & Macnab, R. M. 1980a Proton chemical potential, proton electrical potential and bacterial motility. J. Mol. Biol. 138, 599-614.
63. Khan, S. & Macnab, R. M. 1980b The steady-state counterclockwise/clockwise ratio of bacterial flagellar motors is regulated by protonmotive force. J. Mol. Biol. 138, 563-597.
64. Khan, S., Meister, M. & Berg, H. C. 1985 Constraints on flagellar rotation. J. Mol. Biol. 184, 645-656.
65. Khan, S., Dapice, M. & Reese, T. S. 1988 Effects of mot gene expression on the structure of the flagellar motor. J. Mol. Biol. 202, 575-584.
66. Khan, S., Dapice, M. & Humayun, I. 1990 Energy transduction in the bacterial flagellar motor: effects of load and pH. Biophys. J. 57, 779-796.
67. Khan, S., Khan, I. H. & Reese, T. S. 1991 New structural features of the flagellar base in Salmonella typhimurium revealed by rapid-freeze electron microscopy. J. Bacteriol. 173, 2888-2896.
68. Khan, S., Ivey, D. M. & Krulwich, T. A. 1992 Membrane ultrastructure of alkaliphilic Bacillus species studied by rapid-freeze electron microscopy. J. Bacteriol. 174, 5123-5126.
69. Kihara, M., Francis, N. R., DeRosier, D. J. & Macnab, R. M. 1996 Analysis of a FliM-FliN flagellar switch fusion mutant of Salmonella typhimurium. J. Bacteriol. 178, 4582-4589.
70. Kojima, S., Atsumi, T., Muramoto, K., Kudo, S., Kawagishi, I. & Homma, M. 1997 Vibrio alginolyticus mutants resistant to phenamil, a specific inhibitor of the sodium-driven flagellar motor. J. Mol. Biol. 265, 310-318.
71. +-driven flagellar motor resistant to phenamil, an amiloride analogue, caused by mutations in putative channel components. J. Mol. Biol. 285, 1537-1547.
72. Kubori, T., Shimamoto, N., Yamaguchi, S., Namba, K. & Aizawa, S.-I. 1992 Morphological pathway of flagellar assembly in Salmonella typhimurium. J. Mol. Biol. 226, 433-446.
73. Kubori, T., Yamaguchi, S. & Aizawa, S.-I. 1997 Assembly of the switch complex onto the MS ring complex of Salmonella typhimurium does not require any other flagellar proteins. J. Bacteriol. 179, 813-817.
74. Kutsukake, K., Minamino, T. & Yokoseki, T. 1994 Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J. Bacteriol. 176, 7625-7629.
75. Larsen, S. H., Adler, J., Gargus, J. J. & Hogg, R. W. 1974 Chemomechanical coupling without ATP: the source of energy for motility and chemotaxis in bacteria. Proc. Natl Acad. Sci. USA 71, 1239-1243.
76. Läuger, P. 1988 Torque and rotation rate of the bacterial flagellar motor. Biophys. J. 53, 53-65.
77. Läuger, P. & Kleutsch, B. 1990 Microscopic models of the bacterial flagellar motor. Comments Theor. Biol. 2, 99-123.
78. Lloyd, S. A. & Blair, D. F. 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.
79. Lloyd, S. A.,Tang, H.,Wang, X., Billings, S. & Blair, D. F. 1996 Torque generation in the flagellar motor of Escherichia coli: evidence of a direct role for FliG but not for FliM or FliN. J. Bacteriol. 178, 223-231.
80. Lowe, G., Meister, M. & Berg, H. C. 1987 Rapid rotation of flagellar bundles in swimming bacteria. Nature 325, 637-640.
81. Ludwig, W. 1930 Zur Theorie der Flimmerbewegung (Dynamik, Nutzeffekt, Energiebilanz). Z. Vgl. Physiol. 13, 397-504.
82. Macnab, R. M. 1995 Flagellar switch. In Two-component signal transduction (ed. J. A. Hoch & T. J. Silhavy), pp. 181-199. Washington, DC: American Society for Microbiology.
83. Magariyama, Y., Sugiyama, S., Muramoto, K., Maekawa, Y., Kawagishi, I., Imae, Y. & Kudo, S. 1994 Very fast flagellar rotation. Nature 371, 752.
84. Malakooti, J., Ely, B. & Matsumura, P. 1994 Molecular characterization, nucleotide sequence, and expression of the fliO, fliP, fliQ and fliR genes of Escherichia coli. J. Bacteriol. 176, 189-197.
85. Manson, M. D., Tedesco, P., Berg, H. C., Harold, F. M. & Van der Drift, C. 1977 A protonmotive force drives bacterial flagella. Proc. Natl Acad. Sci. USA 74, 3060-3064.
86. Manson, M. D., Tedesco, P. M. & Berg, H. C. 1980 Energetics of flagellar rotation in bacteria. J. Mol. Biol. 138, 541-561.
87. Matsuura, S., Shioi, J.-I. & Imae, Y. 1977 Motility in Bacillus subtilis driven by an artificial protonmotive force. FEBS Lett. 82, 187-190.
88. Matsuura, S., Shioi, J.-I., Imae, Y. & Iida, S. 1979 Characterization of the Bacillus subtilis motile system driven by an artificially created proton motive force. J. Bacteriol. 140, 28-36.
89. Meister, M. & Berg, H. C. 1987 The stall torque of the bacterial flagellar motor. Biophys. J. 52, 413-419.
90. Meister, M., Lowe, G. & Berg, H. C. 1987 The proton flux through the bacterial flagellar motor. Cell 49, 643-650.
91. Meister, M., Caplan, S. R. & Berg, H. C. 1989 Dynamics of a tightly coupled mechanism for flagellar rotation. Biophys. J. 55, 905-914.
92. Mitchell, P. 1956 Hypothetical thermokinetic and electrokinetic mechanisms of locomotion in micro-organisms. Proc. R. Phys. Soc. Edinb. 25, 32-34.
93. Mitchell, P. 1972 Self-electrophoretic locomotion in microorganisms: bacterial flagella as giant ionophores. FEBS Lett. 28, 1-4.
94. Muramoto, K., Kawagishi, I., Kudo, S., Magariyama, Y., Imae, Y. & Homma, M. 1995 High-speed rotation and speed stability of the sodium-driven flagellar motor in Vibrio alginolyticus. J. Mol. Biol. 251, 50-58.
95. Ohnishi, K., Ohio, Y., Aizawa, S.-I., Macnab, R. M. & Iino, T. 1994 FlgD is a scaffolding protein needed for flagellar hook assembly in Salmonella typhimurium. J. Bacteriol. 176, 2272-2281.
96. Ohnishi, K., Fan, F., Schoenhals, G. J., Kihara, M. & Macnab, R. M. 1997 The FliO, FliP, FliQ, and FliR proteins of Salmonella typhimurium: putative components for flagellar assembly. J. Bacteriol. 179, 6092-6099.
97. Okino, H., Isomura, M., Yamaguchi, S., Magariyama, Y., Kudo, S. & Aizawa, S.-I. 1989 Release of flagellar filament-hook rod complex by a Salmonella typhimurium mutant defective in the M ring of the basal body. J. Bacteriol. 171, 2075-2082.
98. Purcell, E. M. 1977 Life at low Reynolds number. Am. J. Phys. 45, 3-11.
99. Ravid, S. & Eisenbach, M. 1984 Minimal requirements for rotation of bacterial flagella. J. Bacteriol. 158, 1208-1210.
100. Ridgway, H. F., Silverman, M. & Simon, M. I. 1977 Localization of proteins controlling motility and chemotaxis in Escherichia coli. J. Bacteriol. 132, 657-665.
101. Samuel, A. D. T. & Berg, H. C. 1995 Fluctuation analysis of rotational speeds of the bacterial flagellar motor. Proc. Natl Acad. Sci. USA 92, 3502-3506.
102. Samuel, A. D. T. & Berg, H. C. 1996 Torque-generating units of the bacterial flagellar motor step independently. Biophys. J. 71, 918-923.
103. Schoenhals, G. J. & Macnab, R. M. 1996 Physiological and biochemical analyses of FlgH, a lipoprotein forming the outer membrane L ring of the flagellar basal body of Salmonella typhimurium. J. Bacteriol. 178, 4200-4207.
104. Sharp, L. L., Zhou, J. & Blair, D. F. 1995a Features of MotA proton channel structure revealed by tryptophan-scanning mutagenesis. Proc. Natl Acad. Sci. USA 92, 7946-7950.
105. Sharp, L. L., Zhou, J. & Blair, D. F. 1995b Tryptophan-scanning mutagnesis of Mot B, an integral membrane protein essential for flagellar rotation in Escherichia coli. Biochemistry 34, 9166-9171.
106. Shioi, J.-I., Matsuura, S. & Imae, Y. 1980 Quantitative measurements of protonmotive force and motility in Bacillus subtilis. J. Bacteriol. 144, 891-897.
107. Silverman, M. & Simon, M. 1974 Flagellar rotation and the mechanism of bacterial motility. Nature 249, 73-74.
108. Skulachev, V. P. 1975 Electric generators in coupling membranes: direct measurements of the electrogenic activity, molecular mechanisms and some specific functions. In Enzymes, electron transport systems; proceedings of the tenth FEBS meeting, vol. 40 (ed. P. Desnuelle & A. M. Michelson), pp. 225-238. Amsterdam: North-Holland.
109. Stader, J., Matsumura, P., Vacante, D., Dean, G. E. & Macnab, R. M. 1986 Nucleotide sequence of the Escherichia coli motB gene and site-limited incorporation of its product into the cytoplasmic membrane. J. Bacteriol. 166, 244-252.
110. +-driven flagellar motors of alkalophilic Bacillus. J. Biol. Chem. 263, 8215-8219.
111. Suzuki, T. & Komeda, Y. 1981 Incomplete flagellar structures in Escherichia coli mutants. J. Bacteriol. 145, 1036-1041.
112. Suzuki, T., Iino, T., Horiguchi, T. & Yamaguchi, S. 1978 Incomplete flagellar structures in nonflagellate mutants of Salmonella typhimurium. J. Bacteriol. 133, 904-915.
113. Svoboda, K., Mitra, P. P. & Block, S. M. 1994 Fluctuation analysis of motor protein movement and single enzyme kinetics. Proc. Natl Acad. Sci. USA 91, 11 782-11 786.
114. Tang, H., Braun, T. F. & Blair, D. F. 1996 Motility protein complexes in the bacterial flagellar motor. J. Mol. Biol. 261, 209-221.
115. Taylor, G. I. 1952 The action of waving cylindrical tails in propelling microscopic organisms. Proc. R. Soc. Lond A 211, 225-239.
116. Ueno, T., Oosawa, K. & Aizawa, S.-I. 1992 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. 227, 672-677.
117. Ueno, T., Oosawa, K. & Aizawa, S.-I. 1994 Domain structures of the MS ring component protein (FliF) of the flagellar basal body of Salmonella typhimurium. J. Mol. Biol. 236, 546-555.
118. Van der Drift, C., Duiverman, J., Bexkens, H. & Krijnen, A. 1975 Chemotaxis of a motile Streptococcus toward sugars and amino acids. J. Bacteriol. 124, 1142-1147.
119. 1, vacuolar, and archaebacterial ATPase subunits. J. Bacteriol. 173, 3564-3572.
120. Washizu, M., Kurahashi, Y., Iochi, H., Kurosawa, O., Aizawa, S.-I., Kudo, S., Magariyama, Y. & Hotani, H. 1993 Dielectrophoretic measurement of bacterial motor characteristics. IEEE Trans. Ind. Applicat. 29, 286-294.
121. Yamaguchi, S., Aizawa, S.-I., Kihara, M., Isomura, M., Jones, C. J. & Macnab, R. M. 1986a Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J. Bacteriol. 168, 1172-1179.
122. Yamaguchi, S., Fujita, H., Ishihara, A., Aizawa, S.-I. & Macnab, R. M. 1986b Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching. J. Bacteriol. 166, 187-193.
123. Zhao, R., Schuster, S. C. & Khan, S. 1995 Structural effects of mutations in Salmonella typhimurium flagellar switch complex. J. Mol. Biol. 251, 400-412.
124. Zhao, R., Pathak, N., Jaffe, H., Reese, T. S. & Khan, S. 1996 FliN is a major structural protein of the C-ring in the Salmonella typhimurium flagellar basal body. J. Mol. Biol. 261, 195-208.
125. Zhou, J. & Blair, D. F. 1997 Residues of the cytoplasmic domain of MotA essential for torque generation in the bacterial flagellar motor. J. Mol. Biol. 273, 428-439.
126. Zhou, J., Fazzio, R. T. & Blair, D. F. 1995 Membrane topology of the MotA protein of Escherichia coli. J. Mol. Biol. 251, 237-242.
127. Zhou, J., Lloyd, S. A. & Blair, D. F. 1998a Electrostatic interactions between rotor and stator in the bacterial flagellar motor. Proc. Natl Acad. Sci. USA 95, 6436-6441.
128. Zhou, J., Sharp. L. L., Tang, H. L., Lloyd, S. A., Billings, S., Braun, T. F. & Blair, D. F. 1998b Function of protonatable residues in the flagellar motor of Escherichia coli: a critical role for Asp 32 of MotB. J. Bacteriol. 180, 2729-2735.