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F1 rotary motor of ATP synthase is driven by the torsionally-asymmetric drive shaft.

Published version
Peer-reviewed

Type

Article

Change log

Authors

Kulish, O 
Wright, AD 
Terentjev, EM 

Abstract

F1F0 ATP synthase (ATPase) either facilitates the synthesis of ATP in a process driven by the proton moving force (pmf), or uses the energy from ATP hydrolysis to pump protons against the concentration gradient across the membrane. ATPase is composed of two rotary motors, F0 and F1, which compete for control of their shared γ -shaft. We present a self-consistent physical model of F1 motor as a simplified two-state Brownian ratchet using the asymmetry of torsional elastic energy of the coiled-coil γ -shaft. This stochastic model unifies the physical concepts of linear and rotary motors, and explains the stepped unidirectional rotary motion. Substituting the model parameters, all independently known from recent experiments, our model quantitatively reproduces the ATPase operation, e.g. the 'no-load' angular velocity is ca. 400 rad/s anticlockwise at 4 mM ATP. Increasing the pmf torque exerted by F0 can slow, stop and overcome the torque generated by F1, switching from ATP hydrolysis to synthesis at a very low value of 'stall torque'. We discuss the motor efficiency, which is very low if calculated from the useful mechanical work it produces - but is quite high when the 'useful outcome' is measured in the number of H(+) pushed against the chemical gradient.

Description

Keywords

Adenosine Triphosphatases, Adenosine Triphosphate, Bacteria, Molecular Motor Proteins, Phospholipid Transfer Proteins, Proton-Translocating ATPases, Torque

Journal Title

Sci Rep

Conference Name

Journal ISSN

2045-2322
2045-2322

Volume Title

6

Publisher

Springer Science and Business Media LLC
Sponsorship
Engineering and Physical Sciences Research Council (EP/F032773/1)
Engineering and Physical Sciences Research Council (EP/J017639/1)
The authors have benefited from extensive discussions with J. R. Blundell, C. Prior, and G. Fraser, as well as the conceptual input from J. E. Walker (who has originally suggested that the torsional energy of the γ–shaft might be asymmetric). This work has been funded by the {100 + 100 + 100} program by the Ukrainian Government, and the EPSRC Critical Mass Grant for Cambridge Theoretical Condensed Matter EP/J017639.