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

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 (Em) 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 Em(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 Em(TyrZ) caused by the rearrangement of the water molecules at the Ca2+ binding moiety upon the depletion of Ca2+.