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(2). 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(4)CaO(5) cluster in the resting (dark‐stable) S(1) state adopts orientational Jahn–Teller isomeric forms arising from a directional change in electronic configuration of the “dangler” Mn(III) ion. The isomers are consistent with available structural data and explain previously unresolved electron paramagnetic resonance spectroscopic observations on the S(1) state. This unique isomerism in the resting state is shown to be the electronic origin of valence isomerism in the S(2) state, establishing a functional role of orientational Jahn–Teller isomerism unprecedented in biological or artificial catalysis.