He Chen, G. Charles Dismukes, David A. Case

Photosystem II (PSII) of photosynthetic organisms converts light energy into chemical energy by oxidizing water to dioxygen at the Mn4CaO5 oxygen-evolving complex (OEC). Extensive structural data have been collected on the resting dark state (nominally S1 in the standard Kok nomenclature) from crystal diffraction and EXAFS studies but the protonation and Mn oxidation states are still uncertain. A "high-oxidation" model assigns the S1 state to have the formal Mn oxidation level of (III, IV, IV, III), whereas the "low-oxidation" model posits two additional electrons. Generally, additional protons are expected to be associated with the low-oxidation model and were not fully investigated until now. Here we consider structural features of the S0 and S1 states using a quantum mechanics/molecular mechanics (QM/MM) method. We systematically alter the hydrogen-bonding network and the protonation states of bridging and terminal oxygens and His337 to investigate how they influence Mn-Mn and Mn-O distances, relative energetics, and the internal distribution of Mn oxidation states, in both high and low-oxidation state paradigms. The bridging oxygens (O1, O2, O3, O4) all need to be deprotonated (O2-) to be compatible with available structural data, whereas the position of O5 (bridging Mn3, Mn4, and Ca) in the XFEL structure is more consistent with an OH- under the low paradigm. We show that structures with two short Mn-Mn distances, which are sometimes argued to be diagnostic of a high oxidation state paradigm, can also arise in low oxidation-state models. We conclude that the low Mn oxidation state proposal for the OEC can closely fit all of the available structural data at accessible energies in a straightforward manner. Modeling at the 4 H+ protonation level of S1 under the high paradigm predicts rearrangement of bidentate D1-Asp170 to H-bond to O5 (OH-), a geometry found in artificial OEC catalysts.