Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis

Based on new Rhodopseudomonas (Rp.) viridis reaction center (RC) coordinates with a reliable structure of the secondary acceptor quinone (Q(B)) site, a continuum dielectric model and finite difference technique have been used to identify clusters of electrostatically interacting ionizable residues. Twenty-three residues within a distance of 25 Angstrom from Q(B) (Q(B) cluster) have been shown to be strongly electrostatically coupled to Q(B), either directly or indirectly. An analogous cluster of 24 residues is found to interact with Q(A) (Q(A) cluster). Both clusters extend to the cytoplasmic surface in at least two directions. However, the Q(B) cluster differs from the Q(A) cluster in that it has a surplus of acidic residues, more strong electrostatic interactions, is less solvated, and experiences a strong positive electrostatic field arising from the polypeptide backbone. Consequently, upon reduction of Q(A) or Q(B), it is the Q(B) cluster, and not the Q(A) cluster, which is responsible for substoichiometric proton uptake at neutral pH. The bulk of the changes in the Q(B) cluster are calculated to be due to the protonation of a tightly coupled cluster of the three Glu residues (L212, H177, and M234) within the Q(B) cluster. If the lifetime of the doubly reduced state Q(B)(2-) is, long enough, Asp M43 and Ser L223 are predicted to also become protonated. The calculated complex titration behavior of the strongly interacting residues of the Q(B) cluster and the resulting electrostatic response to electron transfer may be a common feature in proton-transferring membrane protein complexes.