Dynamics of Proton Transfer to Internal Water during the Photosynthetic Oxygen-Evolving Cycle

In photosynthesis, the light-driven oxidation of water is a sustainable process, which converts solar to chemical energy and produces protons and oxygen. To enable biomimetic strategies, the mechanism of photosynthetic oxygen evolution must be elucidated. Here, we provide information concerning a critical step in the oxygen-evolving, or S-state, cycle. During this S₃-to-S₀ transition, oxygen is produced, and substrate water binds to the manganese-calcium catalytic site. Our spectroscopic and H₂¹⁸O labeling experiments show that this S₃-to-S₀ step is associated with the protonation of an internal water cluster in a hydrogen-bonding network, which contains calcium. When compared to the protonated water cluster, formed during a preceding step, the S₁-to-S₂ transition, the S₃-to-S₀ hydronium ion is likely to be coordinated by additional water molecules. This evidence shows that internal water and the hydrogen bonding network act as a transient proton acceptor at multiple points in the oxygen-evolving cycle.