Requirement of Chloride for the Downhill Electron Transfer Pathway from the Water-Splitting Center in Natural Photosynthesis

Abstract

In photosystem II (PSII), Cl^- is a prerequisite for the second flash-induced oxidation of the Mn₄CaO₅ cluster (the S₂ to S₃ transition). We report proton transfer from the substrate water molecule via D1-Asp61 and electron transfer via redox-active D1-Tyr161 (TyrZ) to the chlorophyll pair in Cl^--depleted PSII using a quantum mechanical/molecular mechanical approach. The low-barrier H-bond formation between the substrate water molecule and D1-Asp61 remained unaffected upon the depletion of Cl^-. However, the binding site, D2-Lys317, formed a salt bridge with D1-Asp61, leading to the inhibition of the subsequent proton transfer. Remarkably, the redox potential (E_m) of S₂/S₃ increased significantly, making electron transfer from S₂ to TyrZ energetically uphill, as observed in Ca²⁺-depleted PSII. The uphill electron transfer pathway was induced by the significant increase in E_m(S₂/S₃) caused by the loss of charge compensation for D2-Lys317 upon the depletion of Cl^-, whereas it was induced by the significant decrease in E_m(TyrZ) caused by the rearrangement of the water molecules at the Ca²⁺ binding moiety upon the depletion of Ca²⁺.