Fluid Mechanical Matching of H +-ATP Synthase Subunit c-Ring with Lipid Membranes Revealed by 2H Solid-State NMR

Abstract

The F 1F 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 2H-solid-state NMR. In the liquid-crystalline state of DMPC, the 2H-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 2H-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 1F o-ATPse molecular motor.