Mutations targeting the C-terminal domain of FliG can disrupt motor assembly in the Na+-driven flagella of vibrio alginolyticus

Journal of Molecular Biology

Volumn 414, Issue 1, 2011, Pages 62-74

  Kojima, Seiji ^a   Nonoyama, Natsumi ^a   Takekawa, Norihiro ^a   Fukuoka, Hajime ^b   Homma, Michio ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

assembly; flagellar motor; FliG; motility; stator complex

Indexed keywords

MEMBRANE PROTEIN; PROTEIN FLIG; PROTEIN POMA; PROTEIN POMB; SODIUM ION; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; CARBOXY TERMINAL SEQUENCE; CELL MOTILITY; CELLULAR DISTRIBUTION; CRYSTAL STRUCTURE; MUTAGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIBRIO ALGINOLYTICUS;

BACTERIA (MICROORGANISMS); THERMOTOGA MARITIMA; VIBRIO ALGINOLYTICUS;

EID: 81055156686     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.09.019     Document Type: Article

References (56)

1. Berg H.C. The rotary motor of bacterial flagella Annu. Rev. Biochem. 72 2003 19 54 (Pubitemid 36930440)
2. Sowa Y., and Berry R.M. Bacterial flagellar motor Q. Rev. Biophys. 41 2008 103 132
3. Terashima H., Kojima S., and Homma M. Flagellar motility in bacteria structure and function of flagellar motor Int. Rev. Cell Mol. Biol. 270 2008 39 85
4. Macnab R.M. How bacteria assemble flagella Annu. Rev. Microbiol. 57 2003 77 100
5. Francis N.R., Sosinsky G.E., Thomas D., and Derosier D.J. Isolation, characterization and structure of bacterial flagellar motors containing the switch complex J. Mol. Biol. 235 1994 1261 1270 (Pubitemid 24148928)
6. Yamaguchi S., Aizawa S., Kihara M., Isomura M., Jones C.J., and Macnab R.M. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium J. Bacteriol. 168 1986 1172 1179 (Pubitemid 17226800)
7. Yamaguchi S., Fujita H., Ishihara H., Aizawa S., and Macnab R.M. Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching J. Bacteriol. 166 1986 187 193 (Pubitemid 16043299)
8. Lloyd S.A., Tang H., Wang X., Billings S., and Blair D.F. 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 1996 223 231 (Pubitemid 26006087)
9. Thomas D.R., Francis N.R., Xu C., and DeRosier D.J. The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium J. Bacteriol. 188 2006 7039 7048 (Pubitemid 44547609)
10. Kihara M., Miller G.U., and Macnab R.M. Deletion analysis of the flagellar switch protein FliG of Salmonella J. Bacteriol. 182 2000 3022 3028 (Pubitemid 30326914)
11. Irikura V.M., Kihara M., Yamaguchi S., Sockett H., and Macnab R.M. Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor J. Bacteriol. 175 1993 802 810 (Pubitemid 23046944)
12. Dean G.D., Macnab R.M., Stader J., Matsumura P., and Burks C. 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 1984 991 999 (Pubitemid 14008511)
13. Stader J., Matsumura P., Vacante D., Dean G.E., and Macnab R.M. Nucleotide sequence of the Escherichia coli MotB gene and site-limited inccorporation of its product into the cytoplasmic membrane J. Bacteriol. 166 1986 244 252 (Pubitemid 16043307)
14. Asai Y., Kojima S., Kato H., Nishioka N., Kawagishi I., and Homma M. Putative channel components for the fast-rotating sodium-driven flagellar motor of a marine bacterium J. Bacteriol. 179 1997 5104 5110 (Pubitemid 27340544)
15. Braun T.F., Al-Mawsawi L.Q., Kojima S., and Blair D.F. Arrangement of core membrane segments in the MotA/MotB proton-channel complex of Escherichia coli Biochemistry 43 2004 35 45 (Pubitemid 38055940)
16. Kojima S., and Blair D.F. Solubilization and purification of the MotA/MotB complex of Escherichia coli Biochemistry 43 2004 26 34 (Pubitemid 38055939)
17. +-driven polar flagellar motor component of Vibrio alginolyticus J. Biol. Chem. 275 2000 5718 5722 (Pubitemid 30115213)
18. +-driven polar flagellar motor of Vibrio alginolyticus J. Biol. Chem. 275 2000 20223 20228 (Pubitemid 30441635)
19. +-driven flagellar motor of Vibrio alginolyticus J. Biochem. (Tokyo) 135 2004 43 51 (Pubitemid 38405160)
20. Reid S.W., Leake M.C., Chandler J.H., Lo C.J., Armitage J.P., and Berry R.M. The maximum number of torque-generating units in the flagellar motor of Escherichia coli is at least 11 Proc. Natl Acad. Sci. USA 103 2006 8066 8071 (Pubitemid 43801053)
21. Zhou J., Sharp L.L., Tang H.L., Lloyd S.A., Billings S., Braun T.F., and Blair D.F. Function of protonatable residues in the flagellar motor of Escherichia coli: a critical role for Asp 32 of MotB J. Bacteriol. 180 1998 2729 2735 (Pubitemid 28213274)
22. +-driven polar flagellum of Vibrio alginolyticus J. Bacteriol. 186 2004 5281 5291 (Pubitemid 39038131)
23. Kojima S., and Blair D.F. Conformational change in the stator of the bacterial flagellar motor Biochemistry 40 2001 13041 13050 (Pubitemid 33026651)
24. + ion and carboxylates of the PomA-PomB stator unit studied by ATR-FTIR spectroscopy Biochemistry 48 2009 11699 11705
25. Lloyd S.A., and Blair D.F. Charged residues of the rotor protein FliG essential for torque generation in the flagellar motor of Escherichia coli J. Mol. Biol. 266 1997 733 744 (Pubitemid 27113213)
26. +-driven flagellar motor J. Mol. Biol. 334 2003 567 583 (Pubitemid 37386355)
27. +-driven flagellar motor component PomA J. Mol. Biol. 320 2002 403 413 (Pubitemid 34722228)
28. Zhou J., and Blair D.F. Residues of the cytoplasmic domain of MotA essential for torque generation in the bacterial flagellar motor J. Mol. Biol. 273 1997 428 439 (Pubitemid 27470296)
29. Zhou J., Lloyd S.A., and Blair D.F. Electrostatic interactions between rotor and stator in the bacterial flagellar motor Proc. Natl Acad. Sci. USA 95 1998 6436 6441 (Pubitemid 28249031)
30. +-driven motors in Escherichia coli J. Bacteriol. 188 2006 1466 1472 (Pubitemid 43228680)
31. +-driven chimeric flagellar motors in Escherichia coli J. Moi. Biol. 376 2008 1251 1259
32. Brown P.N., Hill C.P., and Blair D.F. Crystal structure of the middle and C-terminal domains of the flagellar rotor protein FliG EMBO J. 21 2002 3225 3234 (Pubitemid 34760555)
33. Lee L.K., Ginsburg M.A., Crovace C., Donohoe M., and Stock D. Structure of the torque ring of the flagellar motor and the molecular basis for rotational switching Nature 466 2010 996 1000
34. +-driven stator of the flagellar motor J. Mol. Biol. 351 2005 707 717 (Pubitemid 41111890)
35. Okabe M., Yakushi T., Asai Y., and Homma M. Cloning and characterization of motX, a Vibrio alginolyticus sodium-driven flagellar motor gene J. Biochem. (Tokyo) 130 2001 879 884 (Pubitemid 34024140)
36. Okunishi I., Kawagishi I., and Homma M. Cloning and characterization of motY, a gene coding for a component of the sodium-driven flagellar motor in Vibrio alginolyticus J. Bacteriol. 178 1996 2409 2415 (Pubitemid 26123507)
37. Terashima H., Fukuoka H., Yakushi T., Kojima S., and Homma M. 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 2006 1170 1180 (Pubitemid 44655326)
38. Fukuoka H., Wada T., Kojima S., Ishijima A., and Homma M. Sodium-dependent dynamic assembly of membrane complexes in sodium-driven flagellar motors Mol. Microbiol. 71 2009 825 835
39. Paulick A., Koerdt A., Lassak J., Huntley S., Wilms I., Narberhaus F., and Thormann K.M. Two different stator systems drive a single polar flagellum in Shewanella oneidensis MR-1 Mol. Microbiol. 71 2009 836 850
40. Sowa Y., Rowe A.D., Leake M.C., Yakushi T., Homma M., Ishijima A., and Berry R.M. Direct observation of steps in rotation of the bacterial flagellar motor Nature 437 2005 916 919 (Pubitemid 41486770)
41. Mashimo T., Hashimoto M., Yamaguchi S., and Aizawa S. Temperature-hypersensitive sites of the flagellar switch component FliG in Salmonella enterica serovar typhimurium J. Bacteriol. 189 2007 5153 5160 (Pubitemid 47076061)
42. Homma M., Oota H., Kojima S., Kawagishi I., and Imae Y. Chemotactic responses to an attractant and a repellent by the polar and lateral flagellar systems of Vibrio alginolyticus Microbiology 142 1996 2777 2783 (Pubitemid 26362915)
43. Delalez N.J., Wadhams G.H., Rosser G., Xue Q., Brown M.T., and Dobbie I.M. Signal-dependent turnover of the bacterial flagellar switch protein FliM Proc. Natl Acad. Sci. USA 107 2010 11347 11351
44. Fukuoka H., Inoue Y., Terasawa S., Takahashi H., and Ishijima A. Exchange of rotor components in functioning bacterial flagellar motor Biochem. Biophys. Res. Commun. 394 2010 130 135
45. Kojima S., Shinohara A., Terashima H., Yakushi T., Sakuma M., and Homma M. Insights into the stator assembly of the Vibrio flagellar motor from the crystal structure of MotY Proc. Natl Acad. Sci. USA 105 2008 7696 7701 (Pubitemid 351872701)
46. Morimoto Y.V., Nakamura S., Kami-Ike N., Namba K., and Minamino T. Charged residues in the cytoplasmic loop of MotA are required for stator assembly into the bacterial flagellar motor Mol. Microbiol. 78 2010 1117 1129
47. +-driven flagellar motors J. Mol. Biol. 327 2003 453 463 (Pubitemid 36298714)
48. Kojima S., Imada K., Sakuma M., Sudo Y., Kojima C., and Minamino T. Stator assembly and activation mechanism of the flagellar motor by the periplasmic region of MotB Mol. Microbiol. 73 2009 710 718
49. Kawagishi I., Okunishi I., Homma M., and Imae Y. Removal of the periplasmic DNase before electroporation enhances efficiency of transformation in a marine bacterium Vibrio alginolyticus Microbiology 140 1994 2355 2361 (Pubitemid 24297041)
50. +-driven flagellar motor of Vibrio alginolyticus J. Bacteriol. 192 2010 375 378
51. +-driven flagellar motor components of Vibrio alginolyticus J. Bacteriol. 181 1999 5103 5106 (Pubitemid 29383546)
52. Terauchi T., Terashima H., Kojima S., and Homma M. The critical role of a conserved residue, PomB-F22, in the transmembrane segment of the flagellar stator complex for conducting ions and generating torque Microbiology 157 2011 2422 2432
53. Kusumoto A., Nishioka N., Kojima S., and Homma M. Mutational analysis of the GTP-binding motif of FlhF which regulates the number and placement of the polar flagellum in Vibrio alginolyticus J. Biochem. 146 2009 643 650
54. Atsumi T., Maekawa Y., Yamada T., Kawagishi I., Imae Y., and Homma M. Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolitycus J. Bacteriol. 178 1996 5024 5026 (Pubitemid 26321308)
55. Bartolome B., Jubete Y., Martinez E., and Cruz F.D. Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives Gene 102 1991 75 78
56. BAD promoter J. Bacteriol. 177 1995 4121 4130