Wang Zaining, Chen Yang, Chen Changhui, Zhang Chunxi
Laboratory of Photochemistry, Institute of Chemistry, Chinese Academy of Sciences, Beijing 100190, China.
University of Chinese Academy of Sciences, Beijing 100049, China.
Plant Cell Physiol. 2025 Jun 25. doi: 10.1093/pcp/pcaf067.
The oxygen-evolving center (OEC) of photosystem II (PSII) is a unique Mn4CaO5-cluster that catalyzes the water-splitting reaction to produce electrons, protons, and dioxygen. Recently, the detailed structures of the OEC in different S-states have been revealed by X-ray free electron laser (XFEL). To facilitate understanding the structure-function relationship of the OEC, a series of artificial Mn4CaO4-clusters have been synthesized, which closely mimic the main metal-oxide core and peripheral ligands, as well as the redox properties of the OEC. Herein, we have systematically analyzed the oxidation states of all Mn ions in the structural data of the OEC revealed by XFEL and artificial Mn4CaO4-clusters. It shows that the oxidation states of some Mn ions in structural data of OEC are significantly lower than the expected values in native PSII, suggesting the occurrence of the reduction of high-valent Mn ions induced by XFEL, whereas all Mn ions in artificial Mn4CaO4-clusters have the same oxidation states as those in the S1 state OEC in native PSII. Furthermore, for the first time, we have observed that the missing μ2-O bridge in the artificial Mn4CaO4-cluster can be generated in solution, forming an unstable Mn4CaO5-cluster, which supports that this μ2-O bridge (O4) is exchangeable and may serve as the active site for O-O bond formation in the cluster. These results provide new insights into the catalytic mechanism of the oxygen-evolving reaction in both natural and artificial photosynthesis.
光系统II（PSII）的析氧中心（OEC）是一种独特的Mn4CaO5簇，它催化水分解反应以产生电子、质子和氧气。最近，通过X射线自由电子激光（XFEL）揭示了不同S态下OEC的详细结构。为了便于理解OEC的结构-功能关系，人们合成了一系列人工Mn4CaO4簇，它们紧密模拟了主要的金属氧化物核心和外围配体，以及OEC的氧化还原性质。在此，我们系统地分析了XFEL揭示的OEC结构数据和人工Mn4CaO4簇中所有锰离子的氧化态。结果表明，OEC结构数据中一些锰离子的氧化态明显低于天然PSII中的预期值，这表明XFEL诱导了高价锰离子的还原，而人工Mn4CaO4簇中的所有锰离子与天然PSII中S1态OEC的氧化态相同。此外，我们首次观察到人工Mn4CaO4簇中缺失的μ2-O桥可以在溶液中生成，形成一个不稳定的Mn4CaO5簇，这支持了这个μ2-O桥（O4）是可交换的，可能是簇中O-O键形成的活性位点。这些结果为自然光合作用和人工光合作用中析氧反应的催化机制提供了新的见解。
