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.

The oxygen-evolving center (OEC) in photosynthesis is a unique biological Mn₄CaO₅-cluster that splits water into electrons, protons, and dioxygen. It is a great challenge for chemists to develop a robust and precise mimic of the OEC in the laboratory. Herein, we report the formation of a rare-earth-element-containing Mn₄YO₄-cluster that represents an excellent and robust model of the OEC. The key synthetic precursor, the Mn₃YO₂-cluster, is reported for the first time, which possesses an identical mixed-valence Mn^III₂Mn^IV metal core and a hydrogen-bonding network coordination sphere. This precursor is very reactive and can convert into various compounds in solution. Importantly, it has been found that the presence of organic bases significantly influences the distribution of intermediates and promotes the formation of the Mn₄YO₄-cluster. Meanwhile, two Mn₄YO₄-clusters are described, which closely mimic the main metal-oxide core and peripheral ligands, as well as the oxidation states of the four Mn ions in the OEC, revealing that both the terminal ligands and a bridging carboxylate are variable. This new Mn₄YO₄-cluster displays a remarkable stability in the presence of water in acetonitrile solution. These findings shed new light on the synthesis of rare-earth-element-containing clusters and the rational design of robust artificial water-splitting catalysts, and provide chemical insights into the dynamic structural changes of both biological and artificial clusters.