Calculated protein and proton motions coupled to electron transfer:: Electron transfer from QA- to QB in bacterial photosynthetic reaction centers

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 accepters allows preparation of the ground (all neutral), P(+)Q(A)(-), P(+)Q(B)(-), P(0)Q(A)(-), and P(0)Q(B)(-) states. The calculated proton binding going from ground to other oxidation states and the free energy of electron transfer from QA-QB to form Q(A)Q(B)(-) (Delta G(AB)) compare well with experiment from pH 5 to pH 11. At pH 7 Delta G(AB) is measured as -65 meV and calculated to be -80 meV. With fixed protein positions as in standard electrostatic calculations, Delta G(AB) is +170 meV. At pH 7 approximate to 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.