Spin State as a Marker for the Structural Evolution of Natures Water-Splitting Catalyst

In transition-metal complexes, the geometric structure is intimately connected with the spin state arising from magnetic coupling between the paramagnetic ions. The tetramanganese-calcium cofactor that catalyzes biological water oxidation in photosystem II cycles through five catalytic intermediates, each of which adopts a specific geometric and electronic structure and is thus characterized by a specific spin state. Here, we review spin-structure correlations in Natures water-splitting catalyst. The catalytic cycle of the Mn₄O₅Ca cofactor can be described in terms of spin-dependent reactivity. The lower inactive S states of the catalyst, S₀ and S₁, are characterized by low-spin ground states, S_GS = ¹/₂ and S_GS = 0. This is connected to the open cubane topology of the inorganic core in these states. The S₂ state exhibits structural and spin heterogeneity in the form of two interconvertible isomers and is identified as the spin-switching point of the catalytic cycle. The first S₂ state form is an open cubane structure with a low-spin S_GS = ¹/₂ ground state, whereas the other represents the first appearance of a closed cubane topology in the catalytic cycle that is associated with a higher-spin ground state of S_GS = ⁵/₂. It is only this higher-spin form of the S₂ state that progresses to the activated S₃ state of the catalyst. The structure of this final metastable catalytic state was resolved in a recent report, showing that all manganese ions are six-coordinate. The magnetic coupling is dominantly ferromagnetic, leading to a high-spin ground state of S_GS = 3. The ability of the Mn₄O₅Ca cofactor to adopt two distinct structural and spin-state forms in the S₂ state is critical for water binding in the S₃ state, allowing spin-state crossing from the inactive, low-spin configuration of the catalyst to the activated, high-spin configuration. Here we describe how an understanding of the magnetic properties of the catalyst in all S states has allowed conclusions on the catalyst function to be reached. A summary of recent literature results is provided that constrains the sequence of molecular level events: catalyst/substrate deprotonation, manganese oxidation, and water molecule insertion.