Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Rapid rotation of flagellar bundles in swimming bacteria

Abstract

A bacterial flagellum is driven by a reversible rotary motor1–3. The power input is determined by protonmotive force and proton flux, the power output by torque and speed: interrelationships between these parameters provide important clues to motor mechanisms. Here we describe the relationship between torque and speed at constant protonmotive force. The measurements are analogous to those that could be made by plugging an electric motor into a constant-voltage outlet, varying the external load, and determining the torque delivered at different speeds. We used suspensions of metabolizing cells of a motile Streptococcus, varied the external load by changing the viscosity of the medium, determined motor speed from the frequency of vibration of the cell body, and inferred motor torque from the rate of body rotation. The flagellar bundles rotate more rapidly than formerly supposed, at rates that increase linearly with temperature. The torque delivered by the flagellar motor drops linearly with speed. At high speed, the torque-generating cycle associated with the transfer of one proton appears to dissipate free energy in a series of small steps.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

References

  1. Berg, H. C. & Anderson, R. A. Nature 245, 380–382 (1973).

    ADS  CAS  Article  Google Scholar 

  2. Berg, H. C., Manson, M. D. & Conley, M. P. Symp. Soc. exp. Biol. 35, 1–31 (1982).

    CAS  PubMed  Google Scholar 

  3. Macnab, R. M. & Aizawa, S.-I. A. Rev. Biophys. Bioeng. 13, 51–83 (1984).

    CAS  Article  Google Scholar 

  4. Berg, H. C. Random Walks in Biology, 78–79 (Princeton University Press, New Jersey, 1983).

    Google Scholar 

  5. Reichert, K. Zentr. Bakt. Parasitenkde Ab. 1 Orig. 51, 14–94 (1909).

    Google Scholar 

  6. Berg, H. C. A. Rev. Biophys. Bioeng. 4, 119–136 (1975).

    CAS  Article  Google Scholar 

  7. Lowe, G. thesis Calif. Inst. Technol. (1987).

  8. Berg, H. C. & Turner, L. Nature 278, 349–351 (1979).

    ADS  CAS  Article  Google Scholar 

  9. Schneider, W. R. & Doetsch, R. N. J. Bact. 117, 696–701 (1974).

    CAS  PubMed  Google Scholar 

  10. Khan, S. & Berg, H. C. Cell 32, 913–919 (1983).

    CAS  Article  Google Scholar 

  11. Manson, M. D., Tedesco, P. M. & Berg, H. C. J. molec. Biol. 138, 541–561 (1980).

    CAS  Article  Google Scholar 

  12. Banks, G., Schaefer, D. W. & Alpert, S. S. Biophys. J. 15, 253–261 (1975).

    CAS  Article  Google Scholar 

  13. Maeda, K., Imae, Y., Shioi, J.-I. & Oosawa, F. J. Bact. 127, 1039–1046 (1976).

    CAS  PubMed  Google Scholar 

  14. Miller, J. B. & Koshland, D. E., Jr J. molec. Biol. 111, 183–201 (1977).

    CAS  Article  Google Scholar 

  15. Ishihara, A., Segall, J. E., Block, S. M. & Berg, H. C. J. Bact. 155, 228–237 (1983).

    CAS  PubMed  Google Scholar 

  16. Armstrong, J. B., Adler, J. & Dahl, M. M. J. Bact. 93, 390–398 (1967).

    CAS  PubMed  Google Scholar 

  17. Prigogine, I. Introduction to Thermodynamics of Irreversible Processes 2nd edn (Interscience, New York, 1961).

    MATH  Google Scholar 

  18. Läuger, P. Nature 268, 360–362 (1977).

    ADS  Article  Google Scholar 

  19. Berg, H. C. & Khan, S. in Motility and Recognition in Cell Biology (eds Sund, H. & Veeger, C.) 486–497 (de Gruyer, Berlin, 1983).

    Google Scholar 

  20. Oosawa, F. & Hayashi, S. J. Phys. Soc. Japan 52, 4019–4028 (1983).

    ADS  CAS  Article  Google Scholar 

  21. Angelini, F., Ascoli, C., Frediani, C. & Petracchi, D. Biophys. J. 50, 929–936 (1986).

    ADS  Article  Google Scholar 

  22. Berg, H. C. & Block, S. M. J. gen. Microbiol. 130, 2915–2920 (1984).

    CAS  PubMed  Google Scholar 

  23. Segall, J. E., Ishihara, A. & Berg, H. C. J. Bact. 161, 51–65 (1985).

    CAS  PubMed  Google Scholar 

  24. Berg, H. C. Adv. opt. Elect. Micros. 7, 1–15 (1978).

    Google Scholar 

  25. Reinsch, C. H. Numer. Math. 10, 177–183 (1967).

    MathSciNet  Article  Google Scholar 

  26. Van der Drift, C., Duiverman, J., Bexkens, H. & Krijnen, A. J. Bact. 124, 1142–1147 (1975).

    CAS  PubMed  Google Scholar 

  27. Berg, H. C. & Brown, D. A. Nature 239, 500–504 (1972).

    ADS  CAS  Article  Google Scholar 

  28. Tirado, M. M. & de la Torre, J. G. J. chem. Phys. 71, 2581–2587 (1979).

    ADS  CAS  Article  Google Scholar 

  29. Tirado, M. M. & de la Torre, J. G. J. chem. Phys. 73, 1986–1993 (1980).

    ADS  CAS  Article  Google Scholar 

  30. Heimbrook, M. E., Wang, W. L. L. & Campbell, G. Abstracts of the Annual Meeting of the American Society for Microbiology, 1986, 240 (American Society for Microbiology, Wash ington DC, 1986).

    Google Scholar 

  31. Berg, H. C. in Cell Motility Vol. 3C (eds Goldman, R., Pollard, T. & Rosenbaum, J.) 47–56 (Cold Spring Harbor Laboratory, New York, 1976).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lowe, G., Meister, M. & Berg, H. Rapid rotation of flagellar bundles in swimming bacteria. Nature 325, 637–640 (1987). https://doi.org/10.1038/325637a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/325637a0

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing