High-resolution structure and mechanism of an F/V-hybrid rotor ring in a Na⁺-coupled ATP synthase.
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.
Department of Structural Biology, Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany.
Doreen
D
Matthies
Theoretical Molecular Biophysics Section, National Heart, Lung and Blood Institute, National Institutes of Health, Building 5635FL, Suite T-800, Bethesda, Maryland 20892, USA.
Wenchang
W
Zhou
Department of Structural Biology, Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany.
Adriana L
AL
Klyszejko
Theoretical Molecular Biophysics Section, National Heart, Lung and Blood Institute, National Institutes of Health, Building 5635FL, Suite T-800, Bethesda, Maryland 20892, USA.
Claudio
C
Anselmi
Department of Structural Biology, Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany.
Özkan
Ö
Yildiz
Department of Molecular Microbiology and Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt am Main, Max-von-Laue-Str. 9, 60438 Frankfurt am Main, Germany.
Karsten
K
Brandt
Department of Molecular Microbiology and Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt am Main, Max-von-Laue-Str. 9, 60438 Frankfurt am Main, Germany.
Volker
V
Müller
1] Theoretical Molecular Biophysics Section, National Heart, Lung and Blood Institute, National Institutes of Health, Building 5635FL, Suite T-800, Bethesda, Maryland 20892, USA [2] Cluster of Excellence Macromolecular Complexes, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany.
José D
JD
Faraldo-Gómez
1] Department of Structural Biology, Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany [2] Cluster of Excellence Macromolecular Complexes, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany.
Thomas
T
Meier
D025181:ATP Synthetase Complexes / Q000737:chemistry* / Q000502:physiology*; D045855:Acetobacterium / Q000201:enzymology*; D000244:Adenosine Diphosphate / Q000378:metabolism; D000255:Adenosine Triphosphate / Q000378:metabolism; D003460:Crystallization; D006859:Hydrogen / Q000378:metabolism; D018625:Microscopy, Atomic Force; D008954:Models, Biological; D056004:Molecular Dynamics Simulation; D021122:Protein Subunits / Q000737:chemistry* / Q000502:physiology*; D012964:Sodium / Q000378:metabolism
D021122:Protein Subunits; D000244:Adenosine Diphosphate; D006859:Hydrogen; D000255:Adenosine Triphosphate; D012964:Sodium; D025181:ATP Synthetase Complexes