The cytochrome b6f complex: DFT modeling of the first step of plastoquinol oxidation by the iron-sulfur protein

Abstract In chloroplasts, the cytochrome (Cyt) b6f complex (plastoquinol-plastocyanin-oxidoreductase) provides connectivity between photosystems (PS) II and I, oxidizing plastoquinol (PQH2) formed in PSII and reducing plastocyanin (electron donor to PSI). The overall rate of the intersystem electron transport is determined by PQH2 oxidation by the Cyt b6f complex. In this work, using the DFT method, we have modeled the first step of PQH2 oxidation by the iron-sulfur protein (ISP) of the Cyt b6f complex. The model system contained the iron–sulfur cluster [Fe2S2], surrounding amino acid residues, and 2,3,5-trimethylbenzoquinol (TMBQH2), the tailless analog of PQH2. The energy profiles of the H atom transfer from TMBQH2 to the iron-sulfur protein (ISP) were calculated for two modes of the H-transfer, “diabatic” and “adiabatic”. The energies of transient states were estimated as 18.4 and 14.4 kcal mol−1. The energy effects of the reaction were evaluated as 7.7 and −0.2 kcal mol−1, respectively. The analysis of partial spin densities and electric charges on the atoms of the model system supports the bidirectional mechanism of the H-transfer reaction: an electron is directed to the Fe(1) atom of the [Fe2S2] cluster of the ISP, and a proton is accepted by the Ne atom of the His155 residue liganding the Fe(1) atom. Using the results of DFT computations of the energy profiles for the H-transfer reaction, we estimated the rate constants of quinol oxidation within the framework of the Marcus-Dutton-Crofts approach. Our analysis supports the diabatic model of the H-transfer, which implies that the elementary steps of electron and proton transfer occur much more rapidly than the concomitant changes in the system geometry. The rate constants estimated for this mode of H-transfer are in reasonable agreement with experimental data on the intersystem electron transport in chloroplasts.