Energetic insights into two electron transfer pathways in light-driven energy-converting enzymes

We report redox potentials (E(m)) for one-electron reduction for all chlorophylls in the two electron-transfer branches of water-oxidizing enzyme photosystem II (PSII), photosystem I (PSI), and purple bacterial photosynthetic reaction centers (PbRC). In PSI, E(m) values for the accessory chlorophylls were similar in both electron-transfer branches. In PbRC, the corresponding E(m) value was 170 mV less negative in the active L-branch (B(L)) than in the inactive M-branch (B(M)), favoring B(L)˙(–) formation. This contrasted with the corresponding chlorophylls, Chl(D1) and Chl(D2), in PSII, where E(m)(Chl(D1)) was 120 mV more negative than E(m)(Chl(D2)), implying that to rationalize electron transfer in the D1-branch, Chl(D1) would need to serve as the primary electron donor. Residues that contributed to E(m)(Chl(D1)) < E(m)(Chl(D2)) simultaneously played a key role in (i) releasing protons from the substrate water molecules and (ii) contributing to the larger cationic population on the chlorophyll closest to the Mn(4)CaO(5) cluster (P(D1)), favoring electron transfer from water molecules. These features seem to be the nature of PSII, which needs to possess the proton-exit pathway to use a protonated electron source—water molecules.