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High-resolution structure of the rotor ring of a proton-dependent ATP synthase

Nature Structural & Molecular Biology volume 16, pages 1068–1073 (2009)Cite this article

Abstract

The crystal structure of the c-ring from the proton-coupled F1Fo ATP synthase from Spirulina platensis is shown at 2.1-Å resolution. The ring includes 15 membrane-embedded c subunits forming an hourglass-shaped assembly. The structure demonstrates that proton translocation across the membrane entails protonation of a conserved glutamate located near the membrane center in the c subunit outer helix. The proton is locked in this site by a precise hydrogen bond network reminiscent of that in Na+-dependent ATP synthases. However, the structure suggests that the different coordination chemistry of the bound proton and the smaller curvature of the outer helix drastically enhance the selectivity of the H+ site against other cations, including H3O+. We propose a model for proton translocation whereby the c subunits remain in this proton-locked state when facing the membrane lipid. Proton exchange would occur in a more hydrophilic and electrostatically distinct environment upon contact with the a subunit interface.

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Figure 1: Structure of the c15 ring of the S. platensis ATP synthase.
Figure 2: Proton-binding site.
Figure 3: Structure comparison of the c-rings from S. platensis and I. tartaricus.
Figure 4: Amino acid alignment of c subunits from S. platensis, spinach (Sp.) chloroplast, I. tartaricus and E. coli, and from the K-subunit from E. hirae.
Figure 5: Proposed mechanism of coupled rotation and ion translocation in the proton-dependent F-ATP synthase of S. platensis.

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Acknowledgements

We thank W. Kühlbrandt for support and for critically reading the manuscript and K. Diederichs and A. Terwisscha van Scheltinga for useful discussions and help. The staff of the Swiss Light Source (SLS, PXII) and the European Synchrotron Radiation Facility (ESRF) are acknowledged for their support. We also thank A. Royant (L'Institut de Biologie Structurale (ISB), Grenoble) for help with single-crystal spectroscopy and J. Langer for help with the ESI-MS measurements. This work was supported in parts by the Cluster of Excellence “Macromolecular Complexes” at the Goethe University, Frankfurt (Deutsche Forschungsgemeinschaft (DFG) Project EXC 115) and DFG Collaborative Research Center 807.

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Authors and Affiliations

  1. Department of Structural Biology, Max-Planck Institute of Biophysics, Frankfurt am Main, Germany

    Denys Pogoryelov, Özkan Yildiz & Thomas Meier

  2. Theoretical Molecular Biophysics Group, Max-Planck Institute of Biophysics, Frankfurt am Main, Germany

    José D Faraldo-Gómez

  3. Cluster of Excellence Macromolecular Complexes, Max-Planck Institute of Biophysics, Frankfurt am Main, Germany

    José D Faraldo-Gómez & Thomas Meier

Authors
  1. Denys Pogoryelov
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  2. Özkan Yildiz
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  3. José D Faraldo-Gómez
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  4. Thomas Meier
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Contributions

D.P. performed the experiments; D.P. and Ö.Y. analyzed the crystallographic data; T.M. and D.P. designed and T.M. directed the research project; D.P., Ö.Y., J.-D.F.G. and T.M. analyzed and interpreted the structure, developed the conceptual model and wrote the paper.

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Correspondence to Thomas Meier.

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Pogoryelov, D., Yildiz, Ö., Faraldo-Gómez, J. et al. High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol 16, 1068–1073 (2009). https://doi.org/10.1038/nsmb.1678

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