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 MnCaO cluster (the S to S 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 () of S/S increased significantly, making electron transfer from S to TyrZ energetically uphill, as observed in Ca-depleted PSII. The uphill electron transfer pathway was induced by the significant increase in (S/S) caused by the loss of charge compensation for D2-Lys317 upon the depletion of Cl, whereas it was induced by the significant decrease in (TyrZ) caused by the rearrangement of the water molecules at the Ca binding moiety upon the depletion of Ca.