Fo-driven Rotation in the ATP Synthase Direction against the Force of F1 ATPase in the FoF1 ATP Synthase

J Biol Chem. 2015 Apr 24;290(17):10717-28. doi: 10.1074/jbc.M115.646430. Epub 2015 Feb 24.

Abstract

Living organisms rely on the FoF1 ATP synthase to maintain the non-equilibrium chemical gradient of ATP to ADP and phosphate that provides the primary energy source for cellular processes. How the Fo motor uses a transmembrane electrochemical ion gradient to create clockwise torque that overcomes F1 ATPase-driven counterclockwise torque at high ATP is a major unresolved question. Using single FoF1 molecules embedded in lipid bilayer nanodiscs, we now report the observation of Fo-dependent rotation of the c10 ring in the ATP synthase (clockwise) direction against the counterclockwise force of ATPase-driven rotation that occurs upon formation of a leash with Fo stator subunit a. Mutational studies indicate that the leash is important for ATP synthase activity and support a mechanism in which residues aGlu-196 and cArg-50 participate in the cytoplasmic proton half-channel to promote leash formation.

Keywords: ATP Synthase; F1Fo ATPase; Molecular Motor; Nanodiscs; Proton Transport; Single-molecule Biophysics.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Triphosphate / biosynthesis
  • Amino Acid Sequence
  • Bacterial Proton-Translocating ATPases / chemistry*
  • Bacterial Proton-Translocating ATPases / genetics
  • Bacterial Proton-Translocating ATPases / metabolism*
  • Escherichia coli / enzymology
  • Escherichia coli / genetics
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Protein Conformation
  • Protein Subunits
  • Rotation
  • Sequence Homology, Amino Acid
  • Static Electricity

Substances

  • Escherichia coli Proteins
  • Protein Subunits
  • Adenosine Triphosphate
  • Bacterial Proton-Translocating ATPases
  • Escherichia coli Proton-Translocating ATPase