Journal
JOURNAL OF BIOLOGICAL CHEMISTRY
Volume 292, Issue 41, Pages 17093-17100Publisher
AMER SOC BIOCHEMISTRY MOLECULAR BIOLOGY INC
DOI: 10.1074/jbc.M117.799940
Keywords
ATP synthase; bioenergetics; F0F1-ATPase; proton transport; single-molecule biophysics
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Funding
- National Institutes of Health [R01 GM097510]
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The two opposed rotary molecular motors of the F0F1-ATP synthase work together to provide the majority of ATP in biological organisms. Rotation occurs in 120 degrees power strokes separated by dwells when F-1 synthesizes or hydrolyzes ATP. F-0 and F-1 complexes connect via a central rotor stalk and a peripheral stator stalk. A major unresolved question is the mechanism in which the interaction between subunit-a and rotating subunit-c-ring in the F-0 motor uses the flux of H+ across the membrane to induce clockwise rotation against the force of counterclockwise rotation driven by the F-1-ATPase. In single-molecule measurements of F0F1 embedded in lipid bilayer nanodiscs, we observed that the ability of the F-0 motor to form transient dwells increases with decreasing pH. Transient dwells can halt counterclockwise rotation powered by the F-1-ATPase in steps equivalent to the rotation of single c-subunits in the c-ring of F-0, and can push the common axle shared by the two motors clockwise by as much as one c-subunit. Because the F-0 proton half-channels that access the periplasm and the cytoplasm are exposed to the same pH, these data are consistent with the conclusion that the periplasmic half-channel is more easily protonated in a manner that halts ATPase-driven rotation by blocking ATPase-dependent proton pumping. The fit of transient dwell occurrence to the sum of three Gaussian curves suggests that the asymmetry of the three ATPase-dependent 120 degrees power strokes imposed by the relative positions of the central and peripheral stalks affects c-subunit stepping efficiency.
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