Structural Dynamics of the Oxygen-Evolving Complex of Photosystem II in Water-Splitting Action

Oxygenic photosynthesis in nature occurs via water splitting catalyzed by the oxygen-evolving complex (OEC) of photosystem II. To split water, the OEC cycles through a sequence of oxidation states (S_i, i = 0-4), the structural mechanism of which is not fully understood under physiological conditions. We monitored the OEC in visible-light-driven water-splitting action by using in situ, aqueous-environment surface-enhanced Raman scattering (SERS). In the unexplored low-frequency region of SERS, we found dynamic vibrational signatures of water binding and splitting. Specific snapshots in the dynamic SERS correspond to intermediate states in the catalytic cycle, as determined by density functional theory and isotopologue comparisons. We assign the previously ambiguous protonation configuration of the S₀-S₃ states and propose a structural mechanism of the OEC's catalytic cycle. The findings address unresolved questions about photosynthetic water splitting and introduce spatially resolved, low-frequency SERS as a chemically sensitive tool for interrogating homogeneous catalysis in operando.