Voltage-generated torque drives the motor of the ATP synthase

The mechanism by which ion-flux through the membrane-bound motor module (F-0) induces rotational torque, driving the rotation of the gamma subunit, was probed with a Na+-translocating hybrid ATP synthase, The ATP-dependent occlusion of 1 Na-22(+) per ATP synthase persisted after modification of the c subunit ring with dicyclohexylcarbodiimide (DCCD), when 22Na+ was added first and ATP second, but not if the order of addition was reversed, These results support the model of ATP-driven rotation of the c subunit oligomer (rotor) versus subunit a (stator) that stops when either a Na-22(+)-loaded or a DCCD-modified rotor subunit reaches the Na+-impermeable stator. The ATP synthase with a Na+-permeable stator catalyzed Na-22(+) (out)/Na+ (in)-exchange after reconstitution into proteoliposomes, which was not significantly affected by DCCD modification of the c submit oligomer, but was abolished by the additional presence of ATP or by a membrane potential (Delta Psi) of 90 mV. We propose that in the idling mode of the motor, Na+ ions are shuttled across the membrane by limited back and forth movements of the rotor against the stator. This motional flexibility is arrested if either ATP or Delta Psi induces the switch from idling into a directed rotation, The Propionigenium modestum ATP synthase catalyzed ATP formation with Delta Psi of 60-125 mV but not with Delta pNa(+) of 195 mV, These results demonstrate that electric forces are essential for ATP synthesis and lead to a new concept of rotary-torque generation in the ATP synthase motor.