The Low Oxidation State Paradigm is More Consistent with XFEL Observations of the S₃ → [S₄] → S₀ Transition in Photosystem II

Photosynthetic water splitting catalyzed by the Mn₄CaO_5/6 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_x. However, computational models based on the high oxidation state (HOS) paradigm have failed to explain key XFEL observations, including the apparent loss of O_x 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 S₄ → S₀ 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 O₂ 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.