Tunneling and Nonadiabatic Effects on a Proton-Coupled Electron Transfer Model for the Q_o Site in Cytochrome bc₁

Abstract

Cytochrome bc 1 is a fundamental enzyme for cellular respiration and photosynthesis. This dimeric protein complex catalyzes a proton-coupled electron transfer (PCET) from the reduced coenzyme-Q substrate (Q) to a bimetallic iron− sulfur cluster in the Q o active site. Herein, we combine molecular dynamics simulations of the complete cytochrome bc 1 protein with electronic-structure calculations of truncated models and a semiclassical tunneling theory to investigate the electron−proton adiabaticity of the initial reaction catalyzed in the Q o site. After sampling possible orientations between the Q substrate and a histidine side chain that functions as hydrogen acceptor, we find that a truncated model composed by ubiquinol-methyl and imidazole-iron(III)-sulfide captures the expected changes in oxidation and spin states of the electron donor and acceptor. Diabatic electronic surfaces obtained for this model with multiconfigurational wave function calculations demonstrate that this reaction is electronic nonadiabatic, and proton tunneling is faster than mixing of electronic configurations. These results indicate the formalism that should be used to calculate vibronic couplings and kinetic parameters for the initial reaction in the Q o site of cytochrome bc 1 . This framework for molecular simulation may also be applied to investigate other PCET reactions in the Q-cycle or in various metalloproteins that catalyze proton translocation coupled to redox processes.

Electro-polarization of protein-like substances accelerates trans-cell-wall electron transfer in microbial extracellular respiration

“…Protein-like substances, such as peptidoglycans and membrane proteins composing amino acids or peptide chains, 21 , 22 are the essential components in cells and extracellular polymeric substances (EPS), which play vital roles in microbial respiration. Apart from the typical electro-active proteins (e.g., cytochrome c and Complex III), 23 , 24 amide groups in common protein-like substances also serve as the sites for electron transfer. 25 It was reported that applying electric potential induced the polarity of amide groups to promote the electron transfer of protein-like substances.…”

Applying Dynamic Magnetic Field To Promote Anaerobic Digestion via Enhancing the Electron Transfer of a Microbial Respiration Chain

“…Saura and Kaila found that NADH oxidation in Complex I actually occurred in a PCET pattern . Besides, as the rate-limiting step of the Q cycle in the respiration chain, the proton in quinoline transfers to the histidine side chains of [2Fe-2S] clusters, which was also considered to be a multisite PCET process . Similar to the electrical potential, the electromotive force induced by the DMF electrically stimulated the sludge to strengthen the extracellular respiration and/or interspecies electron change of microorganisms, which might be the reason for the enrichment of electroactive microorganisms.…”

Dissecting Reaction Mechanisms and Catalytic Contributions in Flavoprotein Fumarate Reductases

“…Reduction of FAD involves electron transfer from heme groups in Fcc 3 or from iron–sulfur clusters in other FRD/SDH enzymes. Both cofactors are only capable of one-electron reductions, producing radical (flavosemiquinone) intermediates, often coupled to proton transfers. , Modeling such reduction processes in detail is challenging and out of the scope of the present study.…”

“…Both cofactors are only capable of one-electron reductions, producing radical (flavosemiquinone) intermediates, often coupled to proton transfers. 77,78 Modeling such reduction processes in detail is challenging and out of the scope of the present study.…”