Time-resolved generation of membrane potential by ba3 cytochrome c oxidase from Thermus thermophilus coupled to single electron injection into the O and OH states

Biochim Biophys Acta Bioenerg. 2017 Nov;1858(11):915-926. doi: 10.1016/j.bbabio.2017.08.007. Epub 2017 Aug 12.

Abstract

Two electrogenic phases with characteristic times of ~14μs and ~290μs are resolved in the kinetics of membrane potential generation coupled to single-electron reduction of the oxidized "relaxed" O state of ba3 oxidase from T. thermophilus (O→E transition). The rapid phase reflects electron redistribution between CuA and heme b. The slow phase includes electron redistribution from both CuA and heme b to heme a3, and electrogenic proton transfer coupled to reduction of heme a3. The distance of proton translocation corresponds to uptake of a proton from the inner water phase into the binuclear center where heme a3 is reduced, but there is no proton pumping and no reduction of CuB. Single-electron reduction of the oxidized "unrelaxed" state (OH→EH transition) is accompanied by electrogenic reduction of the heme b/heme a3 pair by CuA in a "fast" phase (~22μs) and transfer of protons in "middle" and "slow" electrogenic phases (~0.185ms and ~0.78ms) coupled to electron redistribution from the heme b/heme a3 pair to the CuB site. The "middle" and "slow" electrogenic phases seem to be associated with transfer of protons to the proton-loading site (PLS) of the proton pump, but when all injected electrons reach CuB the electronic charge appears to be compensated by back-leakage of the protons from the PLS into the binuclear site. Thus proton pumping occurs only to the extent of ~0.1 H+/e-, probably due to the formed membrane potential in the experiment.

Keywords: Catalytic cycle intermediates; Charge transfer steps; Cytochrome c oxidase; Membrane potential; Thermus thermophilus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / isolation & purification
  • Copper / chemistry
  • Cytochrome b Group / chemistry*
  • Cytochrome b Group / isolation & purification
  • Electron Transport
  • Electron Transport Complex IV / chemistry*
  • Electron Transport Complex IV / isolation & purification
  • Electrons*
  • Heme / chemistry
  • Kinetics
  • Membrane Potentials / physiology*
  • Oxidation-Reduction
  • Oxygen / chemistry
  • Protons*
  • Thermodynamics
  • Thermus thermophilus / chemistry*
  • Thermus thermophilus / enzymology

Substances

  • Bacterial Proteins
  • Cytochrome b Group
  • Protons
  • Heme
  • Copper
  • cytochrome ba3
  • Electron Transport Complex IV
  • Oxygen