Spin State as a Marker for the Structural Evolution of Nature’s Water-Splitting Catalyst

• Published in: Inorganic chemistry 2016-01, Vol.55 (2), p.488-501
• Main Authors: Krewald, Vera, Retegan, Marius, Neese, Frank, Lubitz, Wolfgang, Pantazis, Dimitrios A, Cox, Nicholas
• Format: Article
• Language: English
• Subjects: Catalysis; Electron Spin Resonance Spectroscopy; Evolution, Chemical; Manganese - chemistry; Molecular Structure; Spin Labels
• ISSN: 0020-1669; 1520-510X
• DOI: 10.1021/acs.inorgchem.5b02578

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 Nature’s 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, S 0 and S 1, 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 S 2 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 S 2 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 S 2 state that progresses to the “activated” S 3 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 S 2 state is critical for water binding in the S 3 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.