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

Biophys J. 2008 Jun;94(11):4339-47. doi: 10.1529/biophysj.107.123745. Epub 2008 Feb 29.

Abstract

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Computer Simulation
  • Deuterium
  • Lipid Bilayers / chemistry*
  • Magnetic Resonance Spectroscopy
  • Membrane Fluidity*
  • Microfluidics / methods
  • Models, Chemical*
  • Models, Molecular
  • Molecular Motor Proteins / chemistry*
  • Molecular Motor Proteins / ultrastructure*
  • Motion
  • Protein Conformation
  • Protein Subunits / chemistry
  • Proton-Translocating ATPases / chemistry*
  • Proton-Translocating ATPases / ultrastructure*

Substances

  • Lipid Bilayers
  • Molecular Motor Proteins
  • Protein Subunits
  • Deuterium
  • Proton-Translocating ATPases