Calculated protein and proton motions coupled to electron transfer: Electron transfer from Q(A)(-) to Q(B) 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. Chang ing 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 grou nd 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 p H 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 calcu lations, 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 addit ional proton uptake, but shifts in side chain protonation and position occu r throughout the protein. Waters in channels leading from Q(B) to the surfa ce change site occupancy and orientation. A cluster of acids (GluL212, AspL 210, and L213) and SerL223 near Q(B) play important roles. A simplified vie w shows this cluster with a single negative charge (on AspL213 with a hydro gen 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.