From low- to high-potential bioenergetic chains: Thermodynamic constraints of Q-cycle function.
The electrochemical parameters of all cofactors in the supercomplex formed by the Rieske/cytb complex and the SoxM/A-type O2-reductase from the menaquinone-containing Firmicute Geobacillus stearothermophilus were determined by spectroelectrochemistry and EPR redox titrations. All redox midpoint potentials (Em) were found to be lower than those of ubi- or plastoquinone-containing systems by a value comparable to the redox potential difference between the respective quinones. In particular, Em values of +200mV, -360mV, -220mV and -50mV (at pH7) were obtained for the Rieske cluster, heme bL, heme bH and heme ci, respectively. Comparable values of -330mV, -200mV and +120mV for hemes bL, bH and the Rieske cluster were determined for an anaerobic Firmicute, Heliobacterium modesticaldum. Thermodynamic constraints, optimization of proton motive force build-up and the necessity of ROS-avoidance imposed by the rise in atmospheric O2 2.5billionyears ago are discussed as putative evolutionary driving forces resulting in the observed redox upshift. The close conservation of the entire redox landscape between low and high potential systems suggests that operation of the Q-cycle requires the precise electrochemical tuning of enzyme cofactors to the quinone substrate as stipulated in P. Mitchell's hypothesis.
Institut de Biologie Physico-Chimique, Unité Mixte de Recherche 7099, Centre National de la Recherche Scientifique, Université Paris Diderot, 13 Rue Pierre et Marie Curie, 75005 Paris, France. Electronic address: Lbergdoll@mednet.ucla.edu.
Lucie
L
Bergdoll
Centre National de la Recherche Scientifique, Aix-Marseille Univ, Laboratoire de Bioénergétique et Ingénierie des Protéines, Institut de Biologie Structurale et Microbiologie, Unité Propre de Recherche 7281, FR3479, 31 Chemin Joseph-Aiguier, 13402 Marseille Cedex 20, France.
Felix
F
Ten Brink
Centre National de la Recherche Scientifique, Aix-Marseille Univ, Laboratoire de Bioénergétique et Ingénierie des Protéines, Institut de Biologie Structurale et Microbiologie, Unité Propre de Recherche 7281, FR3479, 31 Chemin Joseph-Aiguier, 13402 Marseille Cedex 20, France. Electronic address: nitschke@imm.cnrs.fr.
Wolfgang
W
Nitschke
Institut de Biologie Physico-Chimique, Unité Mixte de Recherche 7099, Centre National de la Recherche Scientifique, Université Paris Diderot, 13 Rue Pierre et Marie Curie, 75005 Paris, France. Electronic address: picot@ibpc.fr.
Daniel
D
Picot
Centre National de la Recherche Scientifique, Aix-Marseille Univ, Laboratoire de Bioénergétique et Ingénierie des Protéines, Institut de Biologie Structurale et Microbiologie, Unité Propre de Recherche 7281, FR3479, 31 Chemin Joseph-Aiguier, 13402 Marseille Cedex 20, France. Electronic address: baymann@imm.cnrs.fr.
Frauke
F
Baymann
D016227:Benzoquinones / Q000378:metabolism*; D004563:Electrochemistry; D004578:Electron Spin Resonance Spectroscopy; D004734:Energy Metabolism; D013816:Thermodynamics
D016227:Benzoquinones; C004532:quinone
Cytochrome bc(1) complex; Electron bifurcation; Great Oxidation Event; Q-cycle; Quinone; Rieske/cytb complex