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Abstract

The Mn₄CaO_x cluster of the oxygen-evolving complex (OEC) in photosystem II, the site of biological water oxidation, adopts different forms as it progresses through the catalytic cycle of S_i states (i = 0–4) and within each S_i state itself. This has been amply documented by spectroscopy, but the structural basis of spectroscopic polymorphism remains debated. The S₂ state is extensively studied by magnetic resonance spectroscopies. In addition to the common type of g ≈ 2 multiline EPR signal attributed to a low-spin (S = 1/2) form of the manganese cluster, other signals at lower fields (g ≥ 4) associated with the S₂ state arise from higher-spin forms. Resolving the structural identity of the high-spin species is paramount for a microscopic understanding of the catalytic mechanism. Hypotheses explored by theoretical studies implicate valence isomerism, proton tautomerism, or coordination change with respect to the low-spin form. Here we analyze structure–property correlations for multiple formulations employing a common high-level protocol based on multiscale models that combine a converged quantum mechanics region embedded within a large protein region treated semiempirically with an extended tight-binding method (DFT/xTB), surpassing conventional quantum mechanics/molecular mechanics (QM/MM) approaches. Our results provide a comprehensive comparison of magnetic topologies, spin states and energetics in relation to experimental observations. Crucial predictions are made about ¹⁴N hyperfine coupling constants and X-ray absorption Mn K-pre-edge features as criteria for discriminating between different models. This study updates our view on a persistent mystery of biological water oxidation, while providing a refined and transferable computational platform for future theoretical studies of the OEC.