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Torque generation and elastic power transmission in the rotary FOF1-ATPase

Abstract

Adenosine triphosphate (ATP), the universal fuel of the cell, is synthesized from adenosine diphosphate (ADP) and inorganic phosphate (Pi) by 'ATP synthase' (FOF1-ATPase). During respiration or photosynthesis, an electrochemical potential difference of protons is set up across the respective membranes. This powers the enzyme's electrical rotary nanomotor (FO), which drives the chemical nanomotor (F1) by elastic mechanical-power transmission, producing ATP with high kinetic efficiency. Attempts to understand in detail the mechanisms of torque generation in this simple and robust system have been both aided and complicated by a wealth of sometimes conflicting data.

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Figure 1: Structural model of FOF1 in the bacterium Escherichia coli.
Figure 2: Tentative reaction scheme of ATP hydrolysis by the chemical rotary motor, F1.
Figure 3: Model structure illustrating the function of the rotary electromotor, FO.

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Acknowledgements

We thank D. Cherepanov and O. Pänke for their contributions to elastic coupling, G. Hikade and H. Kenneweg for technical assistance, and J. Weber for discussions. We acknowledge financial support from Deutsche Forschungsgemeinschaft, Volkswagenstiftung, European Union and Fonds der Chemie.

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Correspondence should be addressed to W.J. (junge@uos.de).

Supplementary information

Supplementary Movie 1 | effects of the motion of F1.

As the central shaft of F1 (subunit Y, yellow) rotates, it changes the conformation of subunits β (red) and α (blue) of the (αβ)3 pseudo-hexagon. The animation is based on the crystal structure of mitochondrial F1 (ref. 10), which was interpolated to cycle the shown copies of subunits β and α through three conformations. Interpolation courtesy of D. Cherepanov, Universität Osnabrück, Osnabrück Germany. (AVI 2403 kb)

Supplementary Movie 2 | Animated conception of how proton flow might generate torque in the electromotor, FO, of the FOF1-ATPase13.

The movie shows the two boundaries of the coupling membrane, subunit a (green) and the ring of subunit c (grey). Each copy of c carries an acid residue, placed approximately in the middle of the membrane that is either protonated (blue) when facing the lipid core or deprotonated (red) when facing a positive residue on subunit a. Two access channels (green tubes) at the interface between a and cn connect the ring with the aqueous phases separated by the membrane. The generation of torque by the interplay of stochastic Brownian rotation of the cn-ring relative to a, the electrostatic constraints and the offset-positioning of the two access channels is detailed in the main text (see also ref. 13). Animation by M. Sauer and W. Junge, Biophysik, Universität Osnabrück, Osnabrück Germany. (AVI 22841 kb)

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Junge, W., Sielaff, H. & Engelbrecht, S. Torque generation and elastic power transmission in the rotary FOF1-ATPase. Nature 459, 364–370 (2009). https://doi.org/10.1038/nature08145

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