Abstract
Cells employ a variety of linear motors, such as myosin1–3, kinesin4 and RNA polymerase5, which move along and exert force on a filamentous structure. But only one rotary motor has been investigated in detail, the bacterial flagellum6 (a complex of about 100 protein molecules7). We now show that a single molecule of F1-ATPase acts as a rotary motor, the smallest known, by direct observation of its motion. A central rotor of radius ∼1 nm, formed by its γ-subunit, turns in a stator barrel of radius ∼5nm formed by three α- and three β-subunits8. F1 ATPase, together with the membrane-embedded proton-conducting unit F0, forms the H+-ATP synthase that reversibly couples transmembrane proton flow to ATP synthesis/hydrolysis in respiring and photosynthetic cells9,10. It has been suggested that the γ-subunit of F1-ATPase rotates within the αβ-hexamer11, a conjecture supported by structural8, biochemical12,13 and spectroscopic14 studies. We attached a fluorescent actin filament to the γ-subunit as a marker, which enabled us to observe this motion directly. In the presence of ATP, the filament rotated for more than 100 revolutions in an anticlockwise direction when viewed from the 'membrane' side. The rotary torque produced reached more than 40 pN nm −l under high load.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Finer, J. T., Simmons, R. M. & Spudich, J. A. Nature 368, 113–119 (1994).
Miyata, H. et al. Biophys. J. 68, 286S–290S (1995).
Ishijima, A. et al. Biochem. Biophys. Res. Commun. 199, 1057–1063 (1995).
Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. Nature 365, 721–727 (1993).
Yin, H. et al. Science 270, 1653–1657 (1995).
Berg, H. C. & Anderson, R. A. Nature 245, 380–382 (1973).
Aizawa, S. & Jones, C. J. Adv. Microb. Physiol. 32, 110–172 (1991).
Abrahams, J. P., Leslie, A. G. W., Lutter, R. & Walker, J. E. Nature 370, 621–628 (1994).
Mitchell, P. Nature 191, 144–148 (1961).
Kagawa, Y. & Racker, E. J. Biol. Chem 241, 2467–2474 (1966).
Boyer, P. D. Biochim. Biophys. Acta 1140, 215–250 (1993).
Duncan, T. M., Bulygin, V. V., Zhou, Y., Hutcheon, M. L. & Cross, R. L. Proc. Natl Acad. Sci. USA 92, 10964–10968 (1995).
Zhou, Y., Duncan, T. M., Bulygin, V. V., Hutcheon, M. L. & Cross, R. L. Biochim. Biophys. Acta 1275, 96–100 (1996).
Sabert, D., Engelbrecht, S. & Junge, W. Nature 381, 623–625 (1996).
Noji, H., Amano, T. & Yoshida, M. J. Bioenerg, Biomemb. 28, 451–457 (1996).
Kunkel, T. A., Bebenek, K. & McClary, J. Meth. Enzymol. 204, 125–139 (1991).
Aggeler, R. & Capaldi, R. A. J. Biol Chem. 271, 13888–13891 (1996).
Yoshida, M., Sone, N., Hirata, H. & Kagawa, Y. J. Biol. Chem. 252, 3480–3485 (1977).
Oosawa, F. & Hayashi, S. Adv. Biophys. 22, 151–183 (1986).
Meister, M., Lowe, G. & Berg, H. C. Cell 49, 643–650 (1987).
Matsui, T. & Yoshida, M. Biochim. Biophys. Acta 1231, 139–146 (1995).
Harada, Y., Sakurada, K., Aoki, T., Thomas, D. D. & Yanagida, T. J. Mol. Biol. 216, 49–68 (1990).
Sase, I., Miyata, H., Corrie, J. E. T., Craik, J. S. & Kinosita Jr, K. Biophys. J. 69, 323–328 (1995).
Hunt, A. J., Gittes, F. & Howard, J. Biophys. J. 67, 766–781 (1994).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Noji, H., Yasuda, R., Yoshida, M. et al. Direct observation of the rotation of F1-ATPase. Nature 386, 299–302 (1997). https://doi.org/10.1038/386299a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/386299a0
This article is cited by
-
Molecular mechanism on forcible ejection of ATPase inhibitory factor 1 from mitochondrial ATP synthase
Nature Communications (2023)
-
Directed proton transfer from Fo to F1 extends the multifaceted proton functions in ATP synthase
Biophysical Reviews (2023)
-
A DNA origami rotary ratchet motor
Nature (2022)
-
Simulating a chemically fueled molecular motor with nonequilibrium molecular dynamics
Nature Communications (2022)
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.