Orientational Jahn-Teller Isomerism in the Dark-Stable State of Nature's Water Oxidase.

The tetramanganese-calcium cluster of the oxygen-evolving complex of photosystem II adopts electronically and magnetically distinct but interconvertible valence isomeric forms in its first light-driven oxidized catalytic state, S . This bistability is implicated in gating the final catalytic states preceding O-O bond formation, but it is unknown how the biological system enables its emergence and controls its effect. Here we show that the Mn CaO cluster in the resting (dark-stable) S state adopts orientational Jahn-Teller isomeric forms arising from a directional change in electronic configuration of the "dangler" Mn ion. The isomers are consistent with available structural data and explain previously unresolved electron paramagnetic resonance spectroscopic observations on the S state. This unique isomerism in the resting state is shown to be the electronic origin of valence isomerism in the S state, establishing a functional role of orientational Jahn-Teller isomerism unprecedented in biological or artificial catalysis.