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In situ structure of the complete Treponema primitia flagellar motor

Abstract

The bacterial flagellar motor is an amazing nanomachine: built from approximately 25 different proteins, it uses an electrochemical ion gradient to drive rotation at speeds of up to 300 Hz (refs 1, 2). The flagellar motor consists of a fixed, membrane-embedded, torque-generating stator and a typically bidirectional, spinning rotor that changes direction in response to chemotactic signals. Most structural analyses so far have targeted the purified rotor3,4, and hence little is known about the stator and its interactions. Here we show, using electron cryotomography of whole cells, the in situ structure of the complete flagellar motor from the spirochaete Treponema primitia at 7 nm resolution. Twenty individual motor particles were computationally extracted from the reconstructions, aligned and then averaged. The stator assembly, revealed for the first time, possessed 16-fold symmetry and was connected directly to the rotor, C ring and a novel P-ring-like structure. The unusually large size of the motor suggested mechanisms for increasing torque and supported models wherein critical interactions occur atop the C ring, where our data suggest that both the carboxy-terminal and middle domains of FliG are found.

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Figure 1: Electron cryotomography of T. primitia and its periplasmic flagellar motor.
Figure 2: Isosurface of the symmetrized average flagellar motor.
Figure 3: The Treponema motor and its comparison with the Salmonella basal body.

References

  1. Kojima, S. & Blair, D. F. The bacterial flagellar motor: structure and function of a complex molecular machine. Int. Rev. Cytol. 233, 93–134 (2004)

    Article  CAS  Google Scholar 

  2. Berg, H. C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72, 19–54 (2003)

    Article  CAS  Google Scholar 

  3. Francis, N. R., Sosinsky, G. E., Thomas, D. & DeRosier, D. J. Isolation, characterization and structure of bacterial flagellar motors containing the switch complex. J. Mol. Biol. 235, 1261–1270 (1994)

    Article  CAS  Google Scholar 

  4. Thomas, D., Morgan, D. G. & DeRosier, D. J. Structures of bacterial flagellar motors from two FliF–FliG gene fusion mutants. J. Bacteriol. 183, 6404–6412 (2001)

    Article  CAS  Google Scholar 

  5. Sosinsky, G. E., Francis, N. R., Stallmeyer, M. J. & DeRosier, D. J. Substructure of the flagellar basal body of Salmonella typhimurium. J. Mol. Biol. 223, 171–184 (1992)

    Article  CAS  Google Scholar 

  6. Stallmeyer, M. J., Hahnenberger, K. M., Sosinsky, G. E., Shapiro, L. & DeRosier, D. J. Image reconstruction of the flagellar basal body of Caulobacter crescentus. J. Mol. Biol. 205, 511–518 (1989)

    Article  CAS  Google Scholar 

  7. Suzuki, H., Yonekura, K. & Namba, K. Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J. Mol. Biol. 337, 105–113 (2004)

    Article  CAS  Google Scholar 

  8. Young, H. S., Dang, H., Lai, Y., DeRosier, D. J. & Khan, S. Variable symmetry in Salmonella typhimurium flagellar motors. Biophys. J. 84, 571–577 (2003)

    Article  ADS  CAS  Google Scholar 

  9. Khan, S., Dapice, M. & Reese, T. S. Effects of mot gene expression on the structure of the flagellar motor. J. Mol. Biol. 202, 575–584 (1988)

    Article  CAS  Google Scholar 

  10. Khan, S., Ivey, D. M. & Krulwich, T. A. Membrane ultrastructure of alkaliphilic Bacillus species studied by rapid-freeze electron microscopy. J. Bacteriol. 174, 5123–5126 (1992)

    Article  CAS  Google Scholar 

  11. Khan, S., Khan, I. H. & Reese, T. S. New structural features of the flagellar base in Salmonella typhimurium revealed by rapid-freeze electron microscopy. J. Bacteriol. 173, 2888–2896 (1991)

    Article  CAS  Google Scholar 

  12. Coulton, J. W. & Murray, R. G. Cell envelope associations of Aquaspirillum serpens flagella. J. Bacteriol. 136, 1037–1049 (1978)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Yonekura, K. et al. Electron cryomicroscopic visualization of PomA/B stator units of the sodium-driven flagellar motor in liposomes. J. Mol. Biol. 357, 73–81 (2006)

    Article  CAS  Google Scholar 

  14. Braun, T. F., Al-Mawsawi, L. Q., Kojima, S. & Blair, D. F. Arrangement of core membrane segments in the MotA/MotB proton-channel complex of Escherichia coli. Biochemistry 43, 35–45 (2004)

    Article  CAS  Google Scholar 

  15. Limberger, R. J. The periplasmic flagellum of spirochetes. J. Mol. Microbiol. Biotechnol. 7, 30–40 (2004)

    Article  CAS  Google Scholar 

  16. Jackson, S. & Black, S. H. Ultrastructure of Treponema pallidum Nichols following lysis by physical and chemical methods. II. Axial filaments. Arch. Mikrobiol. 76, 325–340 (1971)

    Article  CAS  Google Scholar 

  17. Katayama, E., Shiraishi, T., Oosawa, K., Baba, N. & Aizawa, S. Geometry of the flagellar motor in the cytoplasmic membrane of Salmonella typhimurium as determined by stereo-photogrammetry of quick-freeze deep-etch replica images. J. Mol. Biol. 255, 458–475 (1996)

    Article  CAS  Google Scholar 

  18. Charon, N. W. & Goldstein, S. F. Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu. Rev. Genet. 36, 47–73 (2002)

    Article  CAS  Google Scholar 

  19. Brown, P. N., Hill, C. P. & Blair, D. F. Crystal structure of the middle and C-terminal domains of the flagellar rotor protein FliG. EMBO J. 21, 3225–3234 (2002)

    Article  CAS  Google Scholar 

  20. Lowder, B. J., Duyvesteyn, M. D. & Blair, D. F. FliG subunit arrangement in the flagellar rotor probed by targeted cross-linking. J. Bacteriol. 187, 5640–5647 (2005)

    Article  CAS  Google Scholar 

  21. Leadbetter, J. R., Schmidt, T. M., Graber, J. R. & Breznak, J. A. Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283, 686–689 (1999)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank E. Matson for growing the T. primitia cultures. This work was supported, in part, by NIH grants to G.J.J., a DOE grant to G.J.J., a Searle Scholar Award to G.J.J., an NSF grant to J.R.L., an NIH graduate fellowship to G.E.M., and gifts to Caltech from the Ralph M. Parsons Foundation, the Agouron Institute, and the Gordon and Betty Moore Foundation. Author Contributions G.E.M. collected and analysed the data, and drafted the text and figures; J.R.L. provided cells and discourse; and G.J.J. guided the research and manuscript editing throughout.

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Correspondence to Grant J. Jensen.

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The averaged and symmetrized structure has been deposited in the EM Data Bank (http://www.ebi.ac.uk/msd/index.html) with the accession code EMD-1235. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

Supplementary Figures and Legends 1-5; Supplementary Video Legend; Supplementary Methods; Supplementary Notes. (PDF 620 kb)

Supplementary Video

The movie shows the reconstruction of a single intact T. primitia cell and its periplasmic flagella in three-dimensions, plus the average flagellar motor structure and its presumed rotation. (MOV 77676 kb)

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Murphy, G., Leadbetter, J. & Jensen, G. In situ structure of the complete Treponema primitia flagellar motor. Nature 442, 1062–1064 (2006). https://doi.org/10.1038/nature05015

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