Proceedings of the National
Academy of Sciences of the United States of America
Vol. 112, No. 31, Pages 9626-9631, August 4, 2015
doi:10.1073/pnas.1422885112
Originally published at http://www.pnas.org/ on July 20 2015
Simple mechanism
whereby the F1-ATPase motor rotates with near-perfect
chemomechanical energy conversion
Ei-ichiro Saitaa,b,
Toshiharu Suzukia,b,c, Kazuhiko Kinosita, Jr.c,
and Masasuke Yoshidaa,b,1
aDepartment of Molecular Bioscience, Kyoto Sangyo University,
Kamigamo Motoyama, Kyoto 603-8555, Japan;
bInternational Cooperative Research Project, ATP Synthesis
Regulation Project, Japan Science and Technology Agency, Aomi 2-3-6,
Tokyo 135-0064, Japan;
cDepartment of Physics, Faculty of Science and Engineering,
Waseda University, Shinjuku-ku, Tokyo 169-8555, Japan
1To whom correspondence should be addressed.
Edited by Martin
Karplus, Harvard University, Cambridge, MA, and approved June 23, 2015
(received for review December 1, 2014)
Abstract
F1-ATPase is a motor enzyme in which a central shaft γ
subunit rotates 120° per ATP in the cylinder made of α3β3
subunits. During rotation, the chemical energy of ATP hydrolysis (ΔGATP)
is converted almost entirely into mechanical work by an elusive
mechanism. We measured the force for rotation (torque) under various ΔGATP
conditions as a function of rotation angles of the γ subunit with
quasi-static, single-molecule manipulation and estimated mechanical
work (torque × traveled angle) from the area of the function. The
torque functions show three sawtooth-like repeats of a steep jump and
linear descent in one catalytic turnover, indicating a simple physical
model in which the motor is driven by three springs aligned along a
120° rotation angle. Although the second spring is unaffected by ΔGATP,
activation of the first spring (timing of the torque jump) delays at
low [ATP] (or high [ADP]) and activation of the third spring delays at
high [Pi]. These shifts decrease the size and area of the sawtooth
(magnitude of the work). Thus, F1-ATPase responds to the
change of ΔGATP by shifting the torque jump timing and uses
ΔGATP for the mechanical work with near-perfect efficiency.
Significance
ATP synthase produces most of the ATP in respiratory and
photosynthetic cells. It is a rotary motor enzyme and its catalytic
portion F1-ATPase hydrolyzes ATP to drive rotation of the
central γ subunit. Efficiency of chemomechanical energy conversion by
this motor is always near-perfect under different ATP hydrolysis energy
(ΔGATP) conditions. However, the mechanism for the efficient
conversion remains unknown. We measured the torque as a function of
rotation angle under different ΔGATP conditions and
estimated mechanical work. The torque profiles show three sawtooth-like
repeats during a single ATP hydrolysis. When concentrations of ATP/ADP
and Pi in the environment are changed, the height, and hence the area,
of the sawtooth changes accordingly so that mechanical work can always
match ΔGATP.