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

Abstract

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 Mn₄CaO₅ 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.