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 Mn 4 CaO 5 cluster (the S 2 to S 3 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 S 2 /S 3 increased significantly, making electron transfer from S 2 to TyrZ energetically uphill, as observed in Ca 2+ -depleted PSII. The uphill electron transfer pathway was induced by the significant increase in E m (S 2 /S 3 ) 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 Ca 2+ binding moiety upon the depletion of Ca 2+ .