TY - JOUR
T1 - Theoretical Description of the Primary Proton-Coupled Electron Transfer Reaction in the Cytochrome bc1Complex
AU - Barragan, Angela M.
AU - Soudackov, Alexander V.
AU - Luthey-Schulten, Zaida
AU - Hammes-Schiffer, Sharon
AU - Schulten, Klaus
AU - Solov'Yov, Ilia A.
N1 - Publisher Copyright:
© 2021 American Chemical Society.
PY - 2021/1/20
Y1 - 2021/1/20
N2 - The cytochrome bc1 complex is a transmembrane enzymatic protein complex that plays a central role in cellular energy production and is present in both photosynthetic and respiratory chain organelles. Its reaction mechanism is initiated by the binding of a quinol molecule to an active site, followed by a series of charge transfer reactions between the quinol and protein subunits. Previous work hypothesized that the primary reaction was a concerted proton-coupled electron transfer (PCET) reaction because of the apparent absence of intermediate states associated with single proton or electron transfer reactions. In the present study, the kinetics of the primary bc1 complex PCET reaction is investigated with a vibronically nonadiabatic PCET theory in conjunction with all-atom molecular dynamics simulations and electronic structure calculations. The computed rate constants and relatively high kinetic isotope effects are consistent with experimental measurements on related biomimetic systems. The analysis implicates a concerted PCET mechanism with significant hydrogen tunneling and nonadiabatic effects in the bc1 complex. Moreover, the employed theoretical framework is shown to serve as a general strategy for describing PCET reactions in bioenergetic systems.
AB - The cytochrome bc1 complex is a transmembrane enzymatic protein complex that plays a central role in cellular energy production and is present in both photosynthetic and respiratory chain organelles. Its reaction mechanism is initiated by the binding of a quinol molecule to an active site, followed by a series of charge transfer reactions between the quinol and protein subunits. Previous work hypothesized that the primary reaction was a concerted proton-coupled electron transfer (PCET) reaction because of the apparent absence of intermediate states associated with single proton or electron transfer reactions. In the present study, the kinetics of the primary bc1 complex PCET reaction is investigated with a vibronically nonadiabatic PCET theory in conjunction with all-atom molecular dynamics simulations and electronic structure calculations. The computed rate constants and relatively high kinetic isotope effects are consistent with experimental measurements on related biomimetic systems. The analysis implicates a concerted PCET mechanism with significant hydrogen tunneling and nonadiabatic effects in the bc1 complex. Moreover, the employed theoretical framework is shown to serve as a general strategy for describing PCET reactions in bioenergetic systems.
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U2 - 10.1021/jacs.0c07799
DO - 10.1021/jacs.0c07799
M3 - Article
C2 - 33397104
AN - SCOPUS:85099614197
SN - 0002-7863
VL - 143
SP - 715
EP - 723
JO - Journal of the American Chemical Society
JF - Journal of the American Chemical Society
IS - 2
ER -