Energetics of proton release on the first oxidation step in the water-oxidizing enzyme

In photosystem II (PSII), the Mn(4)CaO(5) cluster catalyses the water splitting reaction. The crystal structure of PSII shows the presence of a hydrogen-bonded water molecule directly linked to O4. Here we show the detailed properties of the H-bonds associated with the Mn(4)CaO(5) cluster using a quantum mechanical/molecular mechanical approach. When O4 is taken as a μ-hydroxo bridge acting as a hydrogen-bond donor to water539 (W539), the S(0) redox state best describes the unusually short O4–O(W539) distance (2.5 Å) seen in the crystal structure. We find that in S(1), O4 easily releases the proton into a chain of eight strongly hydrogen-bonded water molecules. The corresponding hydrogen-bond network is absent for O5 in S(1). The present study suggests that the O4-water chain could facilitate the initial deprotonation event in PSII. This unexpected insight is likely to be of real relevance to mechanistic models for water oxidation.