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F1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits

Nature Structural & Molecular Biology volume 14, pages 841–846 (2007)Cite this article

A Corrigendum to this article was published on 01 October 2007

This article has been updated

Abstract

F1-ATPase, the catalytic part of FoF1-ATP synthase, rotates the central γ subunit within the α3β3 cylinder in 120° steps, each step consuming a single ATP molecule. However, how the catalytic activity of each β subunit is coordinated with the other two β subunits to drive rotation remains unknown. Here we show that hybrid F1 containing one or two mutant β subunits with altered catalytic kinetics rotates in an asymmetric stepwise fashion. Analysis of the rotations reveals that for any given β subunit, the subunit binds ATP at 0°, cleaves ATP at ∼200° and carries out a third catalytic event at ∼320°. This demonstrates the concerted nature of the F1 complex activity, where all three β subunits participate to drive each 120° rotation of the γ subunit with a 120° phase difference, a process we describe as a 'sequential three-site mechanism'.

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Figure 1: Preparation and rotation of hybrid F1.
Figure 2: Histograms of pause durations.
Figure 3: Angle distributions of the rotating beads of F1(1 × E190D) at low ATP concentrations.
Figure 4: Illustrations of the rotation model.

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Change history

  • 17 September 2007

    figure 4 (b) replaced

Notes

  1. *NOTE: In the version of this article initially published, the proposed model for coupling the rotation and catalysis of the F1 β subunits to the concerted activity of their active sites shown in Figure 4 was incorrectly drawn. The error has been corrected in the HTML and PDF versions of the article

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Acknowledgements

We thank P.D. Boyer, K. Kinosita Jr., T. Kodama, H. Itoh, H. Noji, Y. Taniguchi and our other colleagues for valuable discussions, K. Shimabukuro (Tokyo Institute of Technology) for providing the plasmid fragments encoding β(E190D), K. Adachi (Waseda University) and R. Yasuda (Duke University) for programming the image-processing software, and P. Karagiannis for carefully revising the manuscript. This work was supported in part by a grant-in-aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (14380313; to E.M.), and T.A. was supported by a Research Fellowship of the Japan Society for the Promotion of Science.

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Author notes

  1. Takayuki Ariga

    Present address: Present address: Department of Physics, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan.,

Authors and Affiliations

  1. Chemical Resources Laboratory, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, 226-8503, Yokohama, Japan

    Takayuki Ariga, Eiro Muneyuki & Masasuke Yoshida

  2. Graduate School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, 565-0871, Osaka, Japan

    Takayuki Ariga

  3. Department of Physics, Faculty of Science and Engineering, Chuo University, Kasuga 1-13-27, Bunkyo-ku, 112-8551, Tokyo, Japan

    Eiro Muneyuki

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T.A. performed all experiments and data analysis. All authors discussed the results and commented on the manuscript.

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Correspondence to Takayuki Ariga.

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Ariga, T., Muneyuki, E. & Yoshida, M. F1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits. Nat Struct Mol Biol 14, 841–846 (2007). https://doi.org/10.1038/nsmb1296

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