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Rotary mechanism of the prokaryotic Vo motor driven by proton motive force

Author

Listed:
  • Jun-ichi Kishikawa

    (Kita-ku
    Suita
    Sakyo-ku)

  • Yui Nishida

    (Kita-ku)

  • Atsuki Nakano

    (Kita-ku)

  • Takayuki Kato

    (Suita)

  • Kaoru Mitsuoka

    (Osaka University)

  • Kei-ichi Okazaki

    (National Institutes of Natural Sciences
    SOKENDAI)

  • Ken Yokoyama

    (Kita-ku)

Abstract

ATP synthases play a crucial role in energy production by utilizing the proton motive force (pmf) across the membrane to rotate their membrane-embedded rotor c-ring, and thus driving ATP synthesis in the hydrophilic catalytic hexamer. However, the mechanism of how pmf converts into c-ring rotation remains unclear. This study presents a 2.8 Å cryo-EM structure of the Vo domain of V/A-ATPase from Thermus thermophilus, revealing precise orientations of glutamate (Glu) residues in the c12-ring. Three Glu residues face a water channel, with one forming a salt bridge with the Arginine in the stator (a/Arg). Molecular dynamics (MD) simulations show that protonation of specific Glu residues triggers unidirectional Brownian motion of the c12-ring towards ATP synthesis. When the key Glu remains unprotonated, the salt bridge persists, blocking rotation. These findings suggest that asymmetry in the protonation of c/Glu residues biases c12-ring movement, facilitating rotation and ATP synthesis.

Suggested Citation

  • Jun-ichi Kishikawa & Yui Nishida & Atsuki Nakano & Takayuki Kato & Kaoru Mitsuoka & Kei-ichi Okazaki & Ken Yokoyama, 2024. "Rotary mechanism of the prokaryotic Vo motor driven by proton motive force," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53504-x
    DOI: 10.1038/s41467-024-53504-x
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    References listed on IDEAS

    as
    1. Mohammad T. Mazhab-Jafari & Alexis Rohou & Carla Schmidt & Stephanie A. Bueler & Samir Benlekbir & Carol V. Robinson & John L. Rubinstein, 2016. "Atomic model for the membrane-embedded VO motor of a eukaryotic V-ATPase," Nature, Nature, vol. 539(7627), pages 118-122, November.
    2. Vinit K. Rastogi & Mark E. Girvin, 1999. "Structural changes linked to proton translocation by subunit c of the ATP synthase," Nature, Nature, vol. 402(6759), pages 263-268, November.
    3. Atsuko Nakanishi & Jun-ichi Kishikawa & Masatada Tamakoshi & Kaoru Mitsuoka & Ken Yokoyama, 2018. "Cryo EM structure of intact rotary H+-ATPase/synthase from Thermus thermophilus," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
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