Mechanism of Proton Transfer through the D1-E65/D2-E312 Gate during Photosynthetic Water Oxidation

In photosystem II, the D1-E65/D2-E312 dyad in the Cl-1 channel has been proposed to play a pivotal role in proton transfer during water oxidation. However, the precise mechanism remains elusive. Here, the proton transfer mechanism within the Cl-1 channel was investigated using quantum mechanics/molecular mechanics calculations. The molecular vibration of the E65/E312 dyad and its deuteration effect revealed that the recently suggested stepwise proton transfer, i.e., initial proton release from the dyad followed by slow reprotonation, does not occur in the Cl-1 channel. Instead, proton transfer is proposed to take place via a conformational change at the E65/E312 dyad, acting as a gate. In its closed form, a proton is trapped within the dyad, preventing forward proton transfer. This closed form converts into the open form, where protonated D1-E65 provides a hydrogen bond to the water network, thereby facilitating fast Grotthuss-type proton transfer.