Calculated Protein and Proton Motions Coupled to Electron Transfer: Electron Transfer from QA- to QB in Bacterial Photosynthetic Reaction Centers

Abstract

Reaction centers from Rhodobacter sphaeroides were subjected to Monte Carlo sampling to determine the Boltzmann distribution of side-chain ionization states and positions and buried water orientation and site occupancy. Changing the oxidation states of the bacteriochlorophyll dimer electron donor (P) and primary (Q_A) and secondary (Q_B) quinone electron acceptors allows preparation of the ground (all neutral), P⁺Q_A^-, P⁺Q_B^-, P⁰Q_A^-, and P⁰Q_B^- states. The calculated proton binding going from ground to other oxidation states and the free energy of electron transfer from Q_A^-Q_B to form Q_AQ_B^- (ΔG_AB) compare well with experiment from pH 5 to pH 11. At pH 7 ΔG_AB is measured as −65 meV and calculated to be −80 meV. With fixed protein positions as in standard electrostatic calculations, ΔG_AB is +170 meV. At pH 7 ≈0.2 H⁺/protein is bound on Q_A reduction. On electron transfer to Q_B there is little additional proton uptake, but shifts in side chain protonation and position occur throughout the protein. Waters in channels leading from Q_B to the surface change site occupancy and orientation. A cluster of acids (GluL212, AspL210, and L213) and SerL223 near Q_B play important roles. A simplified view shows this cluster with a single negative charge (on AspL213 with a hydrogen bond to SerL233) in the ground state. In the Q_B^- state the cluster still has one negative charge, now on the more distant AspL210. AspL213 and SerL223 move so SerL223 can hydrogen bond to Q_B^-. These rearrangements plus other changes throughout the protein make the reaction energetically favorable.