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ATP-driven proton pumps, which are critical to the operation of a cell,maintain cytosolic and organellar pH levels within a narrow functional range.These pumps employ two very different mechanisms: an elaborate rotary mechanismused by V-ATPase H+ pumps, and a simpler alternating access mechanism used byP-ATPase H+ pumps. Why are two different mechanisms used to perform the samefunction? Systematic analysis, without parameter fitting, of kinetic models ofthe rotary, alternating access and other possible mechanisms suggest that, whenthe ratio of protons transported per ATP hydrolyzed exceeds one, theone-at-a-time proton transport by the rotary mechanism is faster than otherpossible mechanisms across a wide range of driving conditions. When the ratiois one, there is no intrinsic difference in the free energy landscape betweenmechanisms, and therefore all mechanisms can exhibit the same kineticperformance. To our knowledge all known rotary pumps have an H+:ATP ratiogreater than one, and all known alternating access ATP-driven proton pumps havea ratio of one. Our analysis suggests a possible explanation for this apparentrelationship between coupling ratio and mechanism. When the conditions underwhich the pump must operate permit a coupling ratio greater than one, therotary mechanism may have been selected for its kinetic advantage. On the otherhand, when conditions require a coupling ratio of one or less, the alternatingaccess mechanism may have been selected for other possible advantages resultingfrom its structural and functional simplicity.

Biophysical comparison of ATP-driven proton pumping mechanisms suggests a kinetic advantage for the rotary process depending on coupling ratio