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

In photosystem II (PSII), the Mn4CaO5 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 Mn4CaO5 cluster using a quantum mechanical/molecular mechanical approach. When O4 is taken as a mu-hydroxo bridge acting as a hydrogen-bond donor to water539 (W539), the S-0 redox state best describes the unusually short O4-OW539 distance (2.5 angstrom) 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.