Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: Evidence for stator ring curvature and rotor/C-ring assembly flexion

Journal of Bacteriology

Volumn 191, Issue 16, 2009, Pages 5026-5036

  Liu, Jun ^a   Lin, Tao ^a   Botkin, Douglas J ^a   McCrum, Erin ^a   Winkler, Hanspeter ^b   Norris, Steven J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR MOTOR;

ANIMAL CELL; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL MUTATION; BORRELIA BURGDORFERI; CELL MEMBRANE; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CRYOELECTRON TOMOGRAPHY; FLAGELLAR MOTOR; FLGI GENE; GENE; GENE SWITCHING; IMAGE ANALYSIS; NONHUMAN; OPTICAL RESOLUTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; SPIROCHETE; THREE DIMENSIONAL IMAGING;

BACTERIAL PROTEINS; BORRELIA BURGDORFERI; CRYOELECTRON MICROSCOPY; DNA TRANSPOSABLE ELEMENTS; ELECTRON MICROSCOPE TOMOGRAPHY; FLAGELLA; MUTAGENESIS; MUTATION; POLYETHYLENE GLYCOLS;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI;

EID: 67749093018     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00340-09     Document Type: Article

References (50)

1. Aizawa, S. I., G. E. Dean, C. J. Jones, R. M. Macnab, and S. Yamaguchi. 1985. Purification and characterization of the flagellar hook-basal body complex of Salmonella typhimurium. J. Bacteriol. 161:836-849.
2. Becker, M., J. Bunikis, B. D. Lade, J. J. Dunn, A. G. Barbour, and C. L. Lawson. 2005. Structural investigation of Borrelia burgdorferi OspB, a bactericidal Fab target. J. Biol. Chem. 280:17363-17370.
3. Berg, H. C. 2003. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72:19-54.
4. Botkin, D. J., A. N. Abbott, P. E. Stewart, P. A. Rosa, H. Kawabata, H. Watanabe, and S. J. Norris. 2006. Identification of potential virulence determinants by Himar1 transposition of infectious Borrelia burgdorferi B31. Infect. Immun. 74:6690-6699.
5. Brown, P. N., M. Terrazas, K. Paul, and D. F. Blair. 2007. Mutational analysis of the flagellar protein FliG: sites of interaction with FliM and implications for organization of the switch complex. J. Bacteriol. 189:305-312.
6. Charon, N. W., and S. F. Goldstein. 2002. Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu. Rev. Genet. 36:47-73.
7. Charon, N. W., S. F. Goldstein, M. Marko, C. Hsieh, L. L. Gebhardt, M. A. Motaleb, C. W. Wolgemuth, R. J. Limberger, and N. Rowe. 2009. The flat-ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J. Bacteriol. 191:600-607.
8. Chun, S. Y., and J. S. Parkinson. 1988. Bacterial motility: membrane topology of the Escherichia coli MotB protein. Science 239:276-278.
9. Coulton, J. W., and R. G. Murray. 1978. Cell envelope associations of Aquaspirillum serpens flagella. J. Bacteriol. 136:1037-1049.
10. Crowther, R. A., and L. A. Amos. 1971. Harmonic analysis of electron microscope images with rotational symmetry. J. Mol. Biol. 60:123-130.
11. 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.
12. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. Weidman, T. Utterback, L. Watthey, L. McDonald, P. Artiach, C. Bowman, S. Garland, C. Fujii, M. D. Cotton, K. Horst, K. Roberts, B. Hatch, H. O. Smith, and J. C. Venter. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
13. Fraser, C. M., S. J. Norris, G. M. Weinstock, O. White, G. G. Sutton, R. Dodson, M. Gwinn, E. K. Hickey, R. Clayton, K. A. Ketchum, E. Sodergren, J. M. Hardham, M. P. McLeod, S. Salzberg, J. Peterson, H. Khalak, D. Richardson, J. K. Howell, M. Chidambaram, T. Utterback, L. McDonald, P. Artiach, C. Bowman, M. D. Cotton, C. Fujii, S. Garland, B. Hatch, K. Horst, K. Roberts, M. Sandusky, J. Weidman, H. O. Smith, and J. C. Venter. 1998. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281:375-388.
14. Fukuoka, H., T. Wada, S. Kojima, A. Ishijima, and M. Homma. 2009. Sodium-dependent dynamic assembly of membrane complexes in sodiumdriven flagellar motors. Mol. Microbiol. 71:825-835.
15. Goldstein, S. F., N. W. Charon, and J. A. Kreiling. 1994. Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc. Natl. Acad. Sci. USA 91:3433-3437.
16. Izard, J., C. E. Hsieh, R. J. Limberger, C. A. Mannella, and M. Marko. 2008. Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J. Struct. Biol. 163:10-17.
17. Josenhans, C., and S. Suerbaum. 2002. The role of motility as a virulence factor in bacteria. Int. J. Med. Microbiol. 291:605-614.
18. Katayama, E., T. Shiraishi, K. Oosawa, N. Baba, and S. Aizawa. 1996. Geometry of the flagellar motor in the cytoplasmic membrane of Salmonella typhimurium as determined by stereo-photogrammetry of quick-freeze deepetch replica images. J. Mol. Biol. 255:458-475.
19. Kawabata, H., S. J. Norris, and H. Watanabe. 2004. BBE02 disruption mutants of Borrelia burgdorferi B31 have a highly transformable, infectious phenotype. Infect. Immun. 72:7147-7154.
20. 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.
21. Kim, E. A., M. Price-Carter, W. C. Carlquist, and D. F. Blair. 2008. Membrane segment organization in the stator complex of the flagellar motor: implications for proton flow and proton-induced conformational change. Biochemistry 47:11332-11339.
22. Kojima, S., and D. F. Blair. 2004. The bacterial flagellar motor: structure and function of a complex molecular machine. Int. Rev. Cytol. 233:93-134.
23. Kojima, S., and D. F. Blair. 2001. Conformational change in the stator of the bacterial flagellar motor. Biochemistry 40:13041-13050.
24. Koster, A. J., R. Grimm, D. Typke, R. Hegerl, A. Stoschek, J. Walz, and W. Baumeister. 1997. Perspectives of molecular and cellular electron tomography. J. Struct. Biol. 120:276-308.
25. Kremer, J. R., D. N. Mastronarde, and J. R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
26. Kudryashev, M., M. Cyrklaff, W. Baumeister, M. M. Simon, R. Wallich, and F. Frischknecht. 2009. Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes. Mol. Microbiol. 71:1415-1434.
27. Leake, M. C., J. H. Chandler, G. H. Wadhams, F. Bai, R. M. Berry, and J. P. Armitage. 2006. Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443:355-358.
28. Liu, J., A. Bartesaghi, M. J. Borgnia, G. Sapiro, and S. Subramaniam. 2008. Molecular architecture of native HIV-1 gp120 trimers. Nature 455:109-113.
29. Liu, J., D. W. Taylor, E. B. Krementsova, K. M. Trybus, and K. A. Taylor. 2006. Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography. Nature 442:208-211.
30. Lucic, V., F. Forster, and W. Baumeister. 2005. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 74:833-865.
31. Macnab, R. M. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
32. Murphy, G. E., J. R. Leadbetter, and G. J. Jensen. 2006. In situ structure of the complete Treponema primitia flagellar motor. Nature 442:1062-1064.
33. Murphy, G. E., E. G. Matson, J. R. Leadbetter, H. C. Berg, and G. J. Jensen. 2008. Novel ultrastructures of Treponema primitia and their implications for motility. Mol. Microbiol. 67:1184-1195.
34. Nascimento, A. L., A. I. Ko, E. A. Martins, C. B. Monteiro-Vitorello, P. L. Ho, D. A. Haake, S. Verjovski-Almeida, R. A. Hartskeerl, M. V. Marques, M. C. Oliveira, C. F. Menck, L. C. Leite, H. Carrer, L. L. Coutinho, W. M. Degrave, O. A. Dellagostin, H. El-Dorry, E. S. Ferro, M. I. Ferro, L. R. Furlan, M. Gamberini, E. A. Giglioti, A. Goes-Neto, G. H. Goldman, M. H. Goldman, R. Harakava, S. M. Jeronimo, I. L. Junqueira-De-Azevedo, E. T. Kimura, E. E. Kuramae, E. G. Lemos, M. V. Lemos, C. L. Marino, L. R. Nunes, R. C. De Oliveira, G. G. Pereira, M. S. Reis, A. Schriefer, W. J. Siqueira, P. Sommer, S. M. Tsai, A. J. Simpson, J. A. Ferro, L. E. Camargo, J. P. Kitajima, J. C. Setubal, and M. A. Van Sluys. 2004. Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J. Bacteriol. 186:2164-2172.
35. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
36. Ren, S. X., G. Fu, X. G. Jiang, R. Zeng, Y. G. Miao, H. Xu, Y. X. Zhang, H. Xiong, G. Lu, L. F. Lu, H. Q. Jiang, J. Jia, Y. F. Tu, J. X. Jiang, W. Y. Gu, Y. Q. Zhang, Z. Cai, H. H. Sheng, H. F. Yin, Y. Zhang, G. F. Zhu, M. Wan, H. L. Huang, Z. Qian, S. Y. Wang, W. Ma, Z. J. Yao, Y. Shen, B. Q. Qiang, Q. C. Xia, X. K. Guo, A. Danchin, I. Saint Girons, R. L. Somerville, Y. M. Wen, M. H. Shi, Z. Chen, J. G. Xu, and G. P. Zhao. 2003. Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 422:888-893.
37. Roujeinikova, A. 2008. Crystal structure of the cell wall anchor domain of MotB, a stator component of the bacterial flagellar motor: implications for peptidoglycan recognition. Proc. Natl. Acad. Sci. USA 105:10348-10353.
38. Seshadri, R., G. S. Myers, H. Tettelin, J. A. Eisen, J. F. Heidelberg, R. J. Dodson, T. M. Davidsen, R. T. DeBoy, D. E. Fouts, D. H. Haft, J. Selengut, Q. Ren, L. M. Brinkac, R. Madupu, J. Kolonay, S. A. Durkin, S. C. Daugherty, J. Shetty, A. Shvartsbeyn, E. Gebregeorgis, K. Geer, G. Tsegaye, J. Malek, B. Ayodeji, S. Shatsman, M. P. McLeod, D. Smajs, J. K. Howell, S. Pal, A. Amin, P. Vashisth, T. Z. McNeill, Q. Xiang, E. Sodergren, E. Baca, G. M. Weinstock, S. J. Norris, C. M. Fraser, and I. T. Paulsen. 2004. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc. Natl. Acad. Sci. USA 101:5646-5651.
39. Sowa, Y., and R. M. Berry. 2008. Bacterial flagellar motor. Q. Rev. Biophys. 41:103-132.
40. Steere, A. C., J. Coburn, and L. Glickstein. 2004. The emergence of Lyme disease. J. Clin. Investig. 113:1093-1101.
41. Stewart, P. E., and P. A. Rosa. 2008. Transposon mutagenesis of the Lyme disease agent Borrelia burgdorferi. Methods Mol. Biol. 431:85-95.
42. Terashima, H., S. Kojima, and M. Homma. 2008. Flagellar motility in bacteria structure and function of flagellar motor. Int. Rev. Cell Mol. Biol. 270:39-85.
43. Thomas, D., D. G. Morgan, and D. J. DeRosier. 2001. Structures of bacterial flagellar motors from two FliF-FliG gene fusion mutants. J. Bacteriol. 183:6404-6412.
44. Thomas, D. R., N. R. Francis, C. Xu, and D. J. DeRosier. 2006. The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:7039-7048.
45. Volkmann, N. 2002. A novel three-dimensional variant of the watershed transform for segmentation of electron density maps. J. Struct. Biol. 138:123-129.
46. Winkler, H., and K. A. Taylor. 2006. Accurate marker-free alignment with simultaneous geometry determination and reconstruction of tilt series in electron tomography. Ultramicroscopy 106:240-254.
47. Winkler, H., P. Zhu, J. Liu, F. Ye, K. H. Roux, and K. A. Taylor. 2009. Tomographic subvolume alignment and subvolume classification applied to myosin V and SIV envelope spikes. J. Struct. Biol. 165:64-77.
48. Yonekura, K., S. Maki-Yonekura, and K. Namba. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643-650.
49. Zhang, J. R., J. M. Hardham, A. G. Barbour, and S. J. Norris. 1997. Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89:275-285.
50. Zhou, J., L. L. Sharp, H. L. Tang, S. A. Lloyd, S. Billings, T. F. Braun, and D. F. Blair. 1998. Function of protonatable residues in the flagellar motor of Escherichia coli: a critical role for Asp 32 of MotB. J. Bacteriol. 180:2729-2735.