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High-resolution structure and mechanism of an F/V-hybrid rotor ring in a Na+-coupled ATP synthase

Author

Listed:
  • Doreen Matthies

    (Max Planck Institute of Biophysics)

  • Wenchang Zhou

    (Theoretical Molecular Biophysics Section, National Heart, Lung and Blood Institute, National Institutes of Health)

  • Adriana L. Klyszejko

    (Max Planck Institute of Biophysics)

  • Claudio Anselmi

    (Theoretical Molecular Biophysics Section, National Heart, Lung and Blood Institute, National Institutes of Health)

  • Özkan Yildiz

    (Max Planck Institute of Biophysics)

  • Karsten Brandt

    (Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt am Main)

  • Volker Müller

    (Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt am Main)

  • José D. Faraldo-Gómez

    (Theoretical Molecular Biophysics Section, National Heart, Lung and Blood Institute, National Institutes of Health
    Cluster of Excellence Macromolecular Complexes)

  • Thomas Meier

    (Max Planck Institute of Biophysics
    Cluster of Excellence Macromolecular Complexes)

Abstract

All rotary ATPases catalyse the interconversion of ATP and ADP-Pi through a mechanism that is coupled to the transmembrane flow of H+ or Na+. Physiologically, however, F/A-type enzymes specialize in ATP synthesis driven by downhill ion diffusion, while eukaryotic V-type ATPases function as ion pumps. To begin to rationalize the molecular basis for this functional differentiation, we solved the crystal structure of the Na+-driven membrane rotor of the Acetobacterium woodii ATP synthase, at 2.1 Å resolution. Unlike known structures, this rotor ring is a 9:1 heteromer of F- and V-type c-subunits and therefore features a hybrid configuration of ion-binding sites along its circumference. Molecular and kinetic simulations are used to dissect the mechanisms of Na+ recognition and rotation of this c-ring, and to explain the functional implications of the V-type c-subunit. These structural and mechanistic insights indicate an evolutionary path between synthases and pumps involving adaptations in the rotor ring.

Suggested Citation

  • Doreen Matthies & Wenchang Zhou & Adriana L. Klyszejko & Claudio Anselmi & Özkan Yildiz & Karsten Brandt & Volker Müller & José D. Faraldo-Gómez & Thomas Meier, 2014. "High-resolution structure and mechanism of an F/V-hybrid rotor ring in a Na+-coupled ATP synthase," Nature Communications, Nature, vol. 5(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms6286
    DOI: 10.1038/ncomms6286
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    Cited by:

    1. Jimyung Moon & Anja Poehlein & Rolf Daniel & Volker Müller, 2024. "Redirecting electron flow in Acetobacterium woodii enables growth on CO and improves growth on formate," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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