S₀-State Model of the Oxygen-Evolving Complex of Photosystem II

Abstract

The S0 → S1 transition of the oxygen-evolving complex (OEC) of photosystem II is one of the least understood steps in the Kok cycle of water splitting. We introduce a quantum mechanics/molecular mechanics (QM/MM) model of the S0 state that is consistent with extended X-ray absorption fine structure spectroscopy and X-ray diffraction data. In conjunction with the QM/MM model of the S1 state, we address the proton-coupled electron-transfer (PCET) process that occurs during the S0 → S1 transition, where oxidation of a Mn center and deprotonation of a μ-oxo bridge lead to a significant rearrangement in the OEC. A hydrogen bonding network, linking the D1-D61 residue to a Mn-bound water molecule, is proposed to facilitate the PCET mechanism.

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn 4 CaO 5 cluster in photosystem II

“…In particular, model 3 has very large deviations in Mn 3 -O5 and Mn 4 -O5 (0.93 and 0.86 Å, respectively). The calculated distances of model 1 are very similar to those in previous QM/MM calculations (18,19). A relatively large deviation of Mn 3 -O5 (−0.44 Å) from the XFEL structure could be attributed to a minor contribution of the S 0 state as previously suggested (20).…”

“…Different protonation states at W2 and O5 as well as high-and low-oxidation states of the Mn ions were assumed in the constructed models (Table 1). Model 1 (W2/O5 = H 2 O/O 2− ) and model 2 (W2/O5 = OH − /O 2− ), which both have high-oxidation states, have been used in many previous DFT and QM/MM studies (10,14,16,(18)(19)(20)22), whereas model 3 (W2/O5 = OH − /H 2 O) and model 4 (W2/O5 = H 2 O/OH − ) have low-oxidation states that previous DFT calculations suggested could fit to the 1.9-and 1.95-Å structures, respectively, revealed by X-ray crystallography (12). A model of a Ca-depleted WOC with the same protonation and oxidation states as model 1 was also calculated (model 5) (Fig.…”

“…High-spin states were assumed in calculations. The protonation states of W2 and O5 were assumed to be H 2 O, OH − , or O 2− following previous studies (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24).…”

“…With the information of atomic coordinates from high-resolution X-ray structures of the WOC, quantum chemical calculation is now a very powerful method in investigation of the water oxidation mechanism (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme.…”

Photocatalytic Water Oxidation by a Mixed‐Valent MnIII3MnIVO3 Manganese Oxo Core that Mimics the Natural Oxygen‐Evolving Center

“…A structural . [4] Photo-induced electron flow within the S 0 !S 4 Kok cycle of the natural PSII-OEC (bottom right). Balls: calcium yellow, carbon dark grey, manganese(III) blue, manganese(IV) light blue, oxygen red; polyhedra: SiO 4 green, WO 6 red.…”