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+.