A Spotlight on the Compatibility between XFEL and Ab Initio Structures of the Oxygen Evolving Complex in Photosystem II

The Mn4CaO5 cluster of photosystem II promotes a crucial step in the oxygenic photosynthesis, namely, the water-splitting reaction. The structure of such cluster in the S1 state of the Kok–Joliot's cycle has been recently resolved by femtosecond X-ray free-electron laser (XFEL) measurements. However, the XFEL results are characterized by appreciable discrepancies with previous X-ray diffraction (XRD), as well as with S1 models based on ab initio calculations. We provide here a unifying picture based on a combined set of DFT-based structures and molecular dynamics simulations of the S0 and S1 states. Our findings indicate that the XFEL results cannot be interpreted on the grounds of a single structure. A combination of two S1 stable isomers together with a minority contribution of the S0 state is necessary to reproduce XFEL results within 0.16 Å.