The Nature of the Short Oxygen–Oxygen Distance in the Mn4CaO6 Complex of Photosystem II Crystals

The O···O distance for a typical H-bond is ∼2.8 Å, whereas the radiation-damage-free structures of photosystem II (PSII), obtained using the X-ray free electron laser (XFEL), shows remarkably short O···O distances of ∼2 Å in the oxygen-evolving Mn 4 CaO 5/6 complex. Herein, we report the protonation/oxidation states of the short O···O atoms in the XFEL structures using a quantum mechanical/molecular mechanical approach. The O5···O6 distance of 1.9 Å is reproduced only when O6 is an unprotonated O radical (O •- ) with Mn(IV) 3 Mn(III), i.e., the S 3 state. The potential energy profile shows a barrier-less energy minimum region when O5···O6 = 1.90-2.05 Å (O •- ↓) or 2.05-2.20 Å (O •- ↑). Formation of such a short O5···O6 distance is not possible when O6 is OH - with Mn(IV) 4 . In the case in which the O5···O6 distance is 1.9 Å, it seems likely that the O radical species exists in the oxygen-evolving complex of the XFEL-S 3 crystals.