J Phys Chem B. 2018 Dec 20;122(50):11868-11882. doi: 10.1021/acs.jpcb.8b08147. Epub 2018 Nov 28.
The catalytic cycle of photosynthetic water oxidation occurs at the MnCaO oxygen-evolving complex (OEC) of photosystem II. Extensive spectroscopic data have been collected on the intermediates, especially the S (Kok) state, although the proton and electron inventories (Mn oxidation states) are still uncertain. The "high oxidation" paradigm assigns S Mn oxidation level (III, IV, IV, IV) or (IV, IV, IV, III), whereas a "low oxidation" paradigm posits two additional electrons. Here, we investigate the geometric (X-ray diffraction, extended X-ray absorption fine structure) and spectroscopic (electron paramagnetic resonance (EPR), electron nuclear double resonance (ENDOR)) properties of the S state using quantum chemical density functional theory calculations, focusing on the neglected low paradigm. Two interconvertible electronic spin configurations are predicted as ground states, producing multiline ( S = 1/2) and broad ( S = 5/2) EPR signals in the low paradigm oxidation state (III, IV, III, III) and with W2 as OH and O5 as OH. They have "open" ( S = 5/2) and "closed" ( S = 1/2) MnCaO-cubane geometries. Other energetically accessible isomers with ground spin states 1/2, 7/2, 9/2, or 11/2 can be obtained through perturbations of hydrogen-bonding networks (e.g., H from His337 to O3 or W2), consistent with experimental observations. Conformers with the low oxidation state configuration (III, IV, IV, II) also become energetically accessible when the protonation states are O5 (OH), W2 (HO), and neutral His337. The configuration with (III, IV, III, III) agrees well with earlier low-temperature EPR and ENDOR interpretations, whereas the Mn-containing configuration agrees partially with recent ENDOR data. However, the low oxidation paradigm does not yield isotropic ligand hyperfine interactions in good agreement with observed values. We conclude that the low Mn oxidation state proposal for the OEC can closely fit most of the available structural and electronic data for S at accessible energies.
光合作用水氧化的催化循环发生在光系统 II 的 MnCaO 氧释放复合物（OEC）上。已经收集了大量关于中间体的光谱数据，特别是 S（Kok）态，尽管质子和电子库存（Mn 氧化态）仍不确定。“高氧化”范式分配 S Mn 氧化水平（III、IV、IV、IV）或（IV、IV、IV、III），而“低氧化”范式假设另外两个电子。在这里，我们使用量子化学密度泛函理论计算研究了 S 态的几何（X 射线衍射、扩展 X 射线吸收精细结构）和光谱（电子顺磁共振（EPR）、电子核双共振（ENDOR））性质，重点关注被忽视的低范式。预测了两种可相互转换的电子自旋构象作为基态，在低范式氧化态（III、IV、III、III）和 W2 作为 OH 和 O5 作为 OH 下产生多线（S=1/2）和宽带（S=5/2）EPR 信号。它们具有“开放”（S=5/2）和“封闭”（S=1/2）MnCaO 立方烷几何形状。通过氢键网络的扰动（例如，从 His337 到 O3 或 W2 的 H），可以获得具有基自旋态 1/2、7/2、9/2 或 11/2 的其他能量上可及的异构体，这与实验观察结果一致。当质子化状态为 O5（OH）、W2（HO）和中性 His337 时，具有低氧化态构型（III、IV、IV、II）的构象也变得能量上可及。具有（III、IV、III、III）构型的与早期低温 EPR 和 ENDOR 解释吻合较好，而含 Mn 的构型部分与最近的 ENDOR 数据吻合。然而，低氧化范式不能产生与观察值吻合较好的各向同性配体超精细相互作用。我们得出结论，对于 OEC，低 Mn 氧化态方案可以很好地拟合大多数可用的 S 结构和电子数据，这些数据在可及的能量范围内。
