CALCULATIONS OF ELECTROSTATIC ENERGIES IN PHOTOSYNTHETIC REACTION CENTERS

The free energies of radical-pair states of photosynthetic bacterial r eaction centers are examined by calculations based on the crystal stru cture of the reaction center from Rhodopseudomonas viridis. The calcul ations focus on the energies of the states P+B-H and P+BH-, where P is a bacteriochlorophyll dimer that serves as an electron donor in the p hotochemical electron-transfer reaction, H is the bacteriopheophytin t hat accepts the electron, and B is a bacteriochlorophyll that may act as an intermediary. Dielectric effects are treated microscopically by evaluating the induced dipoles on the protein atoms and on a grid of p oints representing the surrounding membrane and solvent. Calculations using both the crystallographic coordinates for the protein atoms and molecular-dynamics/free-energy-perturbation simulations are carried ou t with various treatments of the ionizable amino acid residues and wit h several different models of the membrane. Effects of electrolytes in the solvent are included. The dependence of the results on the size o f the protein region that is treated explicitly in the model is examin ed. Calculations that do not include the membrane or solvent are shown to give unstable results that cannot be used to draw conclusions abou t the energies of the radical-pair states. On the other hand, accounti ng properly for the dielectric effects of the protein, membrane, and s olvent makes the calculated free energies relatively insensitive to th e size of the protein model, the charges assigned to the ionizable ami no acid residues, and other details of the treatment. The calculations place P+BH- 6-7 kcal/mol below the excited singlet state of P, in goo d agreement with experimental measurements, and put P+B-H about 3 kcal /mol above P+BH- with an uncertainty of several kilocalories per mole. These results are consistent with the formation of P+B-H as an interm ediate in the charge-separation reaction, although we cannot exclude t he possibility that the reaction proceeds by a superexchange mechanism . Most of the ionized amino acid residues probably are sufficiently we ll screened so that they have only minor electrostatic effects on the energies of the relaxed P+B-H and P+BH- states, but the effects of two arginines and an aspartic acid residue could be significant. Fields f rom other ionized groups could be important on time scales that are sh ort relative to relaxation of the protein and solvent dipoles. If the solvent is assigned a low polarity in order to model a long dielectric relaxation time, the calculated reorganization energies of the electr on-transfer reactions are decreased but our conclusions about the ener getics of the radical-pair states are not changed significantly.