Fluid mechanical matching of H+-ATP synthase subunit c-ring with lipid membranes revealed by 2H solid-state NMR.

The F(1)F(o)-ATP synthase utilizes the transmembrane H(+) gradient for the synthesis of ATP. F(o) subunit c-ring plays a key role in transporting H(+) through F(o) in the membrane. We investigated the interactions of Escherichia coli subunit c with dimyristoylphosphatidylcholine (DMPC-d(54)) at lipid/protein ratios of 50:1 and 20:1 by means of (2)H-solid-state NMR. In the liquid-crystalline state of DMPC, the (2)H-NMR moment values and the order parameter (S(CD)) profile were little affected by the presence of subunit c, suggesting that the bilayer thickness in the liquid-crystalline state is matched to the transmembrane hydrophobic surface of subunit c. On the other hand, hydrophobic mismatch of subunit c with the lipid bilayer was observed in the gel state of DMPC. Moreover, the viscoelasticity represented by a square-law function of the (2)H-NMR relaxation was also little influenced by subunit c in the fluid phase, in contrast with flexible nonionic detergents or rigid additives. Thus, the hydrophobic matching of the lipid bilayer to subunit c involves at least two factors, the hydrophobic length and the fluid mechanical property. These findings may be important for the torque generation in the rotary catalytic mechanism of the F(1)F(o)-ATPse molecular motor.