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  • Featured in Physics
  • Open Access

Efficiently Driving F1 Molecular Motor in Experiment by Suppressing Nonequilibrium Variation

Takahide Mishima1, Deepak Gupta2,3,4, Yohei Nakayama1, W. Callum Wareham4, Takumi Ohyama1, David A. Sivak4,*, and Shoichi Toyabe1,†

  • *Contact author: dsivak@sfu.ca
  • †Contact author: toyabe@tohoku.ac.jp
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Phys. Rev. Lett. 135, 148402 – Published 3 October, 2025

DOI: https://doi.org/10.1103/b24h-v7by

Abstract

F1-ATPase (F1) is central to cellular energy transduction. Forcibly rotated by another motor Fo, F1 catalyzes adenosine triphosphate (ATP) synthesis by converting mechanical work into chemical free energy stored in the molecule ATP. The details of how Fo drives F1 are not fully understood; however, evaluating efficient ways to rotate F1 could provide fruitful insights into this driving since there is a selective pressure to improve efficiency. Here, we show that rotating F1 with an angle clamp is significantly more efficient than a constant torque. Our experiments, combined with theory and simulation, indicate that the angle clamp significantly suppresses the nonequilibrium variation that contributes to the futile dissipation of input work.

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Physics Subject Headings (PhySH)

Focus

How a Molecular Motor Minimizes Energy Waste

Published 3 October, 2025

Turning a biologically important molecular motor at a constant rate saves energy, according to experiments.

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References (36)

  1. C. Bustamante, J. Liphardt, and F. Ritort, Phys. Today 58, No. 7, 43 (2005).
  2. Y. Rondelez, G. Tresset, T. Nakashima, Y. Kato-Yamada, H. Fujita, S. Takeuchi, and H. Noji, Nature (London) 433, 773 (2005).
  3. S. Toyabe, T. Watanabe-Nakayama, T. Okamoto, S. Kudo, and E. Muneyuki, Proc. Natl. Acad. Sci. U.S.A. 108, 17951 (2011).
  4. E.-i. Saita, T. Suzuki, K. Kinosita, and M. Yoshida, Proc. Natl. Acad. Sci. U.S.A. 112, 9626 (2015).
  5. N. Soga, K. Kimura, K. Kinosita, M. Yoshida, and T. Suzuki, Proc. Natl. Acad. Sci. U.S.A. 114, 4960 (2017).
  6. H. Noji, R. Yasuda, M. Yoshida, and K. Kinosita, Nature (London) 386, 299 (1997).
  7. S. Toyabe, T. Sagawa, M. Ueda, E. Muneyuki, and M. Sano, Nat. Phys. 6, 988 (2010).
  8. U. Seifert, Rep. Prog. Phys. 75, 126001 (2012).
  9. L. Peliti and S. Pigolotti, Stochastic Thermodynamics: An Introduction (Princeton University Press, Princeton, NJ, 2021).
  10. S. Oikawa, Y. Nakayama, S. Ito, T. Sagawa, and S. Toyabe, arXiv:2503.01200.
  11. D. Gupta, S. J. Large, S. Toyabe, and D. A. Sivak, J. Phys. Chem. Lett. 13, 11844 (2022).
  12. W. C. Wareham and D. A. Sivak, Phys. Rev. E 111, 064410 (2025).
  13. A. Hahn, J. Vonck, D. J. Mills, T. Meier, and W. Kühlbrandt, Science 360, 620 (2018).
  14. See Supplemental Material at http://link.aps.org/supplemental/10.1103/b24h-v7by for supplementary methods and texts, which includes Ref. [15].
  15. E. Aurell, K. Gawędzki, C. Mejía-Monasterio, R. Mohayaee, and P. Muratore-Ginanneschi, J. Stat. Phys. 147, 487 (2012).
  16. S. Toyabe, H. Ueno, and E. Muneyuki, Europhys. Lett. 97, 40004 (2012).
  17. K. Kawaguchi, S.-i. Sasa, and T. Sagawa, Biophys. J. 106, 2450 (2014).
  18. T. Watanabe-Nakayama, S. Toyabe, S. Kudo, S. Sugiyama, M. Yoshida, and E. Muneyuki, Biochem. Biophys. Res. Commun. 366, 951 (2008).
  19. S. Toyabe, T. Okamoto, T. Watanabe-Nakayama, H. Taketani, S. Kudo, and E. Muneyuki, Phys. Rev. Lett. 104, 198103 (2010).
  20. H. Wang and G. Oster, Europhys. Lett. 57, 134 (2002).
  21. C.-B. Li and S. Toyabe, Biophys. Rev. 12, 419 (2020).
  22. Y. Nakayama and S. Toyabe, Phys. Rev. Res. 7, 023213 (2025).
  23. J. Mehl, B. Lander, C. Bechinger, V. Blickle, and U. Seifert, Phys. Rev. Lett. 108, 220601 (2012).
  24. U. Seifert, Annu. Rev. Condens. Matter Phys. 10, 171 (2019).
  25. G. E. Crooks, Phys. Rev. E 60, 2721 (1999).
  26. T. Harada and S.-i. Sasa, Phys. Rev. Lett. 95, 130602 (2005).
  27. A. C. Barato and U. Seifert, Phys. Rev. Lett. 114, 158101 (2015).
  28. J. M. Horowitz and T. R. Gingrich, Nat. Phys. 16, 599 (2020).
  29. M. W. Jack, N. J. López-Alamilla, and K. J. Challis, Phys. Rev. E 101, 062123 (2020).
  30. T. Schmiedl and U. Seifert, Phys. Rev. Lett. 98, 108301 (2007).
  31. S. Blaber and D. A. Sivak, J. Phys. Comm. 7, 033001 (2023).
  32. D. A. Sivak and G. E. Crooks, Phys. Rev. Lett. 108, 190602 (2012).
  33. S. Tafoya, S. J. Large, S. Liu, C. Bustamante, and D. A. Sivak, Proc. Natl. Acad. Sci. U.S.A. 116, 5920 (2019).
  34. D. Gupta, S. H. L. Klapp, and D. A. Sivak, Phys. Rev. E 108, 024117 (2023).
  35. S. J. Large, R. Chetrite, and D. A. Sivak, Europhys. Lett. 124, 20001 (2018).
  36. www.alliancecan.ca

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Phys. Rev. Lett. 135, 148402– Published 3 October, 2025
  • Received 2 May 2025
  • Accepted 18 August 2025
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Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article’s title, journal citation, and DOI.

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