1887

Abstract

Many bacteria are motile by means of flagella, semi-rigid helical filaments rotated at the filament's base and energized by proton or sodium-ion gradients. Torque is created between the two major components of the flagellar motor: the rotating switch complex and the cell-wall-associated stators, which are arranged in a dynamic ring-like structure. Being motile provides a survival advantage to many bacteria, and thus the flagellar motor should work optimally under a wide range of environmental conditions. Recent studies have demonstrated that numerous species possess a single flagellar system but have two or more individual stator systems that contribute differentially to flagellar rotation. This review describes recent findings on rotor–stator interactions, on the role of different stators, and on how stator selection could be regulated. An emerging model suggests that bacterial flagellar motors are dynamic and can be tuned by stator swapping in response to different environmental conditions.

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2010-05-01
2024-04-25
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References

  1. Armitage J. P. 1999; Bacterial tactic responses. Adv Microb Physiol 41:229–289
    [Google Scholar]
  2. Asai Y., Yakushi T., Kawagishi I., Homma M. 2003; Ion-coupling determinants of Na+-driven and H+-driven flagellar motors. J Mol Biol 327:453–463
    [Google Scholar]
  3. Berg H. C. 2003; The rotary motor of bacterial flagella. Annu Rev Biochem 72:19–54
    [Google Scholar]
  4. Blair D. F., Berg H. C. 1988; Restoration of torque in defective flagellar motors. Science 242:1678–1681
    [Google Scholar]
  5. Block S. M., Berg H. C. 1984; Successive incorporation of force-generating units in the bacterial rotary motor. Nature 309:470–472
    [Google Scholar]
  6. Braun T. F., Al-Mawsawi L. Q., Kojima S., Blair D. F. 2004; Arrangement of core membrane segments in the MotA/MotB proton-channel complex of Escherichia coli. Biochemistry 43:35–45
    [Google Scholar]
  7. Coulton J. W., Murray R. G. 1978; Cell envelope associations of Aquaspirillum serpens flagella. J Bacteriol 136:1037–1049
    [Google Scholar]
  8. Dobell C. 1960 Antony van Leeuwenhoek and His “Little Animals” New York: Dover;
  9. Doyle T. B., Hawkins A. C., McCarter L. L. 2004; The complex flagellar torque generator of Pseudomonas aeruginosa. J Bacteriol 186:6341–6350
    [Google Scholar]
  10. Fukuoka H., Yakushi T., Kusumoto A., Homma M. 2005; Assembly of motor proteins, PomA and PomB, in the Na+-driven stator of the flagellar motor. J Mol Biol 351:707–717
    [Google Scholar]
  11. Fukuoka H., Wada T., Kojima S., Ishijima A., Homma M. 2009; Sodium-dependent dynamic assembly of membrane complexes in sodium-driven flagellar motors. Mol Microbiol 71:825–835
    [Google Scholar]
  12. Gosink K. K., Häse C. C. 2000; Requirements for conversion of the Na+-driven flagellar motor of Vibrio cholerae to the H+-driven motor of Escherichia coli. J Bacteriol 182:4234–4240
    [Google Scholar]
  13. Hosking E. R., Manson M. D. 2008; Clusters of charged residues at the C terminus of MotA and N terminus of MotB are important for function of the Escherichia coli flagellar motor. J Bacteriol 190:5517–5521
    [Google Scholar]
  14. Ito M., Hicks D. B., Henkin T. M., Guffanti A. A., Powers B. D., Zvi L., Uematsu K., Krulwich T. A. 2004; MotPS is the stator-force generator for motility of alkaliphilic Bacillus, and its homologue is a second functional Mot in Bacillus subtilis. Mol Microbiol 53:1035–1049
    [Google Scholar]
  15. Ito M., Terahara N., Fujinami S., Krulwich T. A. 2005; Properties of motility in Bacillus subtilis powered by the H+-coupled MotAB flagellar stator, Na+-coupled MotPS or hybrid stators MotAS or MotPB. J Mol Biol 352:396–408
    [Google Scholar]
  16. 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
    [Google Scholar]
  17. 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
    [Google Scholar]
  18. Koerdt A., Paulick A., Mock M., Jost K., Thormann K. M. 2009; MotX and MotY are required for flagellar rotation in Shewanella oneidensis MR-1. J Bacteriol 191:5085–5093
    [Google Scholar]
  19. Kojima S., Blair D. F. 2004a; The bacterial flagellar motor: structure and function of a complex molecular machine. Int Rev Cytol 233:93–134
    [Google Scholar]
  20. Kojima S., Blair D. F. 2004b; Solubilization and purification of the MotA/MotB complex of Escherichia coli. Biochemistry 43:26–34
    [Google Scholar]
  21. Kojima S., Shinohara A., Terashima H., Yakushi T., Sakuma M., Homma M., Namba K., Imada K. 2008; Insights into the stator assembly of the Vibrio flagellar motor from the crystal structure of MotY. Proc Natl Acad Sci U S A 105:7696–7701
    [Google Scholar]
  22. Kojima S., Imada K., Sakuma M., Sudo Y., Kojima C., Minamino T., Homma M., Namba K. 2009; Stator assembly and activation mechanism of the flagellar motor by the periplasmic region of MotB. Mol Microbiol 73:710–718
    [Google Scholar]
  23. Leake M. C., Chandler J. H., Wadhams G. H., Bai F., Berry R. M., Armitage J. P. 2006; Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443:355–358
    [Google Scholar]
  24. Liu J., Lin T., Botkin D. J., McCrum E., Winkler H., Norris S. J. 2009; Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion. J Bacteriol 191:5026–5036
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. 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
    [Google Scholar]
  27. Macnab R. M. 2003; How bacteria assemble flagella. Annu Rev Microbiol 57:77–100
    [Google Scholar]
  28. Magariyama Y., Sugiyama S., Muramoto K., Maekawa Y., Kawagishi I., Imae Y., Kudo S. 1994; Very fast flagellar rotation. Nature 371:752
    [Google Scholar]
  29. McCarter L. L. 2006; Regulation of flagella. Curr Opin Microbiol 9:180–186
    [Google Scholar]
  30. McCarter L., Hilmen M., Silverman M. 1988; Flagellar dynamometer controls swarmer cell differentiation of Vibrio parahaemolyticus. Cell 54:345–351
    [Google Scholar]
  31. Merino S., Shaw J. G., Tomás J. M. 2006; Bacterial lateral flagella: an inducible flagella system. FEMS Microbiol Lett 263:127–135
    [Google Scholar]
  32. Minamino T., Imada K., Namba K. 2008; Molecular motors of the bacterial flagella. Curr Opin Struct Biol 18:693–701
    [Google Scholar]
  33. Paulick A., Koerdt A., Lassak J., Huntley S., Wilms I., Narberhaus F., Thormann K. M. 2009; Two different stator systems drive a single polar flagellum in Shewanella oneidensis MR-1. Mol Microbiol 71:836–850
    [Google Scholar]
  34. Reid S. W., Leake M. C., Chandler J. H., Lo C. J., Armitage J. P., Berry R. M. 2006; The maximum number of torque-generating units in the flagellar motor of Escherichia coli is at least 11. Proc Natl Acad Sci U S A 103:8066–8071
    [Google Scholar]
  35. Ryu W. S., Berry R. M., Berg H. C. 2000; Torque-generating units of the flagellar motor of Escherichia coli have a high duty ratio. Nature 403:444–447
    [Google Scholar]
  36. Sato K., Homma M. 2000; Functional reconstitution of the Na+-driven polar flagellar motor component of Vibrio alginolyticus. J Biol Chem 275:5718–5722
    [Google Scholar]
  37. Shimada T., Sakazaki R., Suzuki K. 1985; Peritrichous flagella in mesophilic strains of Aeromonas. Jpn J Med Sci Biol 38:141–145
    [Google Scholar]
  38. Sowa Y., Berry R. M. 2008; Bacterial flagellar motor. Q Rev Biophys 41:103–132
    [Google Scholar]
  39. Sowa Y., Rowe A. D., Leake M. C., Yakushi T., Homma M., Ishijima A., Berry R. M. 2005; Direct observation of steps in rotation of the bacterial flagellar motor. Nature 437:916–919
    [Google Scholar]
  40. Terahara N., Fujisawa M., Powers B., Henkin T. M., Krulwich T. A., Ito M. 2006; An intergenic stem-loop mutation in the Bacillus subtilis ccpA- motPS operon increases motPS transcription and the MotPS contribution to motility. J Bacteriol 188:2701–2705
    [Google Scholar]
  41. Terashima H., Fukuoka H., Yakushi T., Kojima S., Homma M. 2006; The Vibrio motor proteins, MotX and MotY, are associated with the basal body of Na+-driven flagella and required for stator formation. Mol Microbiol 62:1170–1180
    [Google Scholar]
  42. Thomas D. R., Francis N. R., Xu C., DeRosier D. J. 2006; The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. J Bacteriol 188:7039–7048
    [Google Scholar]
  43. Toutain C. M., Zegans M. E., O'Toole G. A. 2005; Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J Bacteriol 187:771–777
    [Google Scholar]
  44. Toutain C. M., Caizza N. C., Zegans M. E., O'Toole G. A. 2007; Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. Res Microbiol 158:471–477
    [Google Scholar]
  45. Van Way S. M., Hosking E. R., Braun T. F., Manson M. D. 2000; Mot protein assembly into the bacterial flagellum: a model based on mutational analysis of the motB gene. J Mol Biol 297:7–24
    [Google Scholar]
  46. Wang Q., Suzuki A., Mariconda S., Porwollik S., Harshey R. M. 2005; Sensing wetness: a new role for the bacterial flagellum. EMBO J 24:2034–2042
    [Google Scholar]
  47. Wilhelms M., Vilches S., Molero R., Shaw J. G., Tomas J. M., Merino S. 2009; Two redundant sodium-driven stator motor proteins are involved in Aeromonas hydrophila polar flagellum rotation. J Bacteriol 191:2206–2217
    [Google Scholar]
  48. Yakushi T., Yang J., Fukuoka H., Homma M., Blair D. F. 2006; Roles of charged residues of rotor and stator in flagellar rotation: comparative study using H+-driven and Na+-driven motors in Escherichia coli. J Bacteriol 188:1466–1472
    [Google Scholar]
  49. Yorimitsu T., Homma M. 2001; Na+-driven flagellar motor of Vibrio. Biochim Biophys Acta 150582–93
    [Google Scholar]
  50. Yorimitsu T., Sowa Y., Ishijima A., Yakushi T., Homma M. 2002; The systematic substitutions around the conserved charged residues of the cytoplasmic loop of Na+-driven flagellar motor component PomA. J Mol Biol 320:403–413
    [Google Scholar]
  51. Yorimitsu T., Mimaki A., Yakushi T., Homma M. 2003; The conserved charged residues of the C-terminal region of FliG, a rotor component of the Na+-driven flagellar motor. J Mol Biol 334:567–583
    [Google Scholar]
  52. 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
    [Google Scholar]
  53. Zhou J., Lloyd S. A., Blair D. F. 1998; Electrostatic interactions between rotor and stator in the bacterial flagellar motor. Proc Natl Acad Sci U S A 95:6436–6441
    [Google Scholar]
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