Intermonomer electron transfer in the bc1 complex dimer is controlled by the energized state and by impaired electron transfer between low and high potential hemes

Edited by Peter Brzezinski

Received 19 January 2007; received in revised form 8 March 2007; accepted 9 March 2007. published online 23 March 2007.

Abstract

The cytochrome bc1 complex (commonly called Complex III) is the central enzyme of respiratory and photosynthetic electron transfer chains. X-ray structures have revealed the bc1 complex to be a dimer, and show that the distance between low potential (bL) and high potential (bH) hemes, is similar to the distance between low potential hemes in different monomers. This suggests that electron transfer between monomers should occur at the level of the bL hemes. Here, we show that although the rate constant for bL→bL electron transfer is substantial, it is slow compared to the forward rate from bL to bH, and the intermonomer transfer only occurs after equilibration within the first monomer. The effective rate of intermonomer transfer is about 2-orders of magnitude slower than the direct intermonomer electron transfer.

Abbreviations: bc1 complex, ubiquinol:cytochrome c oxidoreductase, bL and bH, low- and high-potential hemes of cytochrome b, respectively, cyt, cytochrome, Eh, redox potential of the medium, Em, midpoint redox potential, F, the Faraday constant, ISP, Rieske iron–sulfur protein, kapp, apparent rate constant of electron transfer between monomers, KbHQ, the equilibrium constant of electron transfer from cyt bH to Qi,

, the equilibrium constant of electron transfer between bL and bH hemes,

, the equilibrium constant of electron transfer between bL and bH hemes at zero transmembrane potential,

, the intrinsic rate constant of electron transfer between bL and bH hemes in the same monomer,

, the intrinsic rate constant of electron transfer between bL hemes, MET, monomer–monomer electron transfer, Q, coenzyme Q (ubiquinone), QH2, dihydroquinone (ubiquinol), Qi site (Qo site), quinone reducing (quinol oxidizing) site of bc1 complex, r, edge-to-edge distance, R, the gas constant, Rb., Rhodobacter,

, edge-to-edge distance between bL and bH hemes,

, edge-to-edge distance between bL and bH hemes, SQ, semiquinone, T, the absolute temperature, α, the fraction of Δψ applied between bH and bL, γ, the coefficient in Eq. (1), equal to either 4.2, or 3.1, λ, the reorganization energy in eV, Δλ, difference of reorganization energies for the reactions bL

↔

bH and bL

↔

bL, Δψ, transmembrane electric potential, τapp

1/kapp, apparent time of electron transfer between monomers, which takes into account the equilibration within the initial monomer,

, intrinsic time of electron transfer between bL hemes, ΔG∘, the standard reaction free energy in eV

Keywords: Cyt bc1, Complex III, Monomer, Dimer, Electron transfer, Coenzyme Q-10, Ubiquinone, Superoxide

a Department of Biochemistry, University of Illinois at Urbana – Champaign, 156 Davenport Hall, 607 South Mathews Avenue, Urbana, IL 6l801, United States

b Center for Biophysics and Computational Biology, University of Illinois at Urbana – Champaign, 156 Davenport Hall, 607 South Mathews Avenue, Urbana, IL 6l801, United States

Corresponding author. Fax: +1 217 244 6615.

PII: S0014-5793(07)00303-1

doi:10.1016/j.febslet.2007.03.037

2 of 27