Ariafard Alireza, Longhurst Matthew, Swiegers Gerhard F, Stranger Robert
Research School of Chemistry, Australian National University, Canberra, Australia.
Intelligent Polymer Research Institute, University of Wollongong, Wollongong, Australia.
Chemistry. 2025 Jul 8;31(38):e202501010. doi: 10.1002/chem.202501010. Epub 2025 Jun 18.
Photosynthetic water splitting catalyzed by the MnCaO cluster in the oxygen-evolving complex (OEC) of photosystem II (PSII) is crucial for sustaining the supply of oxygen on the Earth. A recent serial femtosecond X-ray crystallography (XFEL) study has provided unprecedented insights into the structural dynamics of the OEC during the S₃ → [S₄] → S₀ transition, revealing that this process involves a peroxide intermediate formed via oxo-oxyl radical coupling between O5 and O. However, computational models based on the high oxidation state (HOS) paradigm have failed to explain key XFEL observations, including the apparent loss of O upon peroxide formation and the largely unchanged Mn4─O5 distance from S₄ to the peroxide intermediate. Here, we apply density functional theory to remodel the S → S transition within the low oxidation state (LOS) paradigm and show that this model yields results more consistent with the XFEL observations. Notably, this study demonstrates that the LOS paradigm can support the formation of an oxyl radical species essential for O─O coupling and subsequent O generation, a capability previously thought to be exclusive to the HOS model. Our findings offer an alternative explanation that complements existing models and broadens our understanding of the OEC mechanism.
由光系统II（PSII）的放氧复合体（OEC）中的MnCaO簇催化的光合水分解对于维持地球上氧气的供应至关重要。最近的一项飞秒X射线晶体学（XFEL）系列研究为OEC在S₃→[S₄]→S₀转变过程中的结构动力学提供了前所未有的见解，揭示了这一过程涉及通过O5和O之间的氧代-氧自由基偶联形成的过氧化物中间体。然而，基于高氧化态（HOS）范式的计算模型未能解释关键的XFEL观测结果，包括过氧化物形成时O的明显损失以及从S₄到过氧化物中间体的Mn4─O5距离基本不变。在这里，我们应用密度泛函理论在低氧化态（LOS）范式内对S→S转变进行重新建模，并表明该模型产生的结果与XFEL观测结果更一致。值得注意的是，这项研究表明LOS范式可以支持形成对于O─O偶联和随后的O生成至关重要的氧自由基物种，这一能力以前被认为是HOS模型所独有的。我们的发现提供了一种补充现有模型的替代解释，并拓宽了我们对OEC机制的理解。
