Orientational Jahn–Teller Isomerism in the Dark‐Stable State of Nature's Water Oxidase

Abstract

The tetramanganese-calcium cluster of the oxygenevolving complex of photosystem II adopts electronically and magnetically distinct but interconvertible valence isomeric forms in its first light-driven oxidized catalytic state,S 2 .T his bistability is implicated in gating the final catalytic states preceding O À Ob ond 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 (darkstable) S 1 state adopts orientational Jahn-Teller isomeric forms arising from adirectional 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.T his unique isomerism in the resting state is shown to be the electronic origin of valence isomerism in the S 2 state,establishing afunctional role of orientational Jahn-Teller isomerism unprecedented in biological or artificial catalysis.

Redox Isomerism in the S3 State of the Oxygen‐Evolving Complex Resolved by Coupled Cluster Theory

“…The Jahn‐Teller axes of the Mn1 III and Mn4 III ions in the peroxo structure are collinear, as in one of the Jahn‐Teller isomeric forms of the resting S 1 state. [40] According to the root mean square deviations (RMSDs) from the XFEL distances (Table S3), the structure that corresponds to the S 3 P isomer is in best agreement with the 5WS6 XFEL model, which has been directly interpreted as a peroxo form, [4b] with an RMSD of 0.21 Å for the 25 atom core structure and 0.12 Å for the Mn atoms only, while the S 3 O models show similar level of RMSD with respect to all XFEL models associated with the S 3 state. In particular, the O5−O6 distance of 1.4 Å observed for S 3 P is identical with the 5WS6 crystallographic model, whereas the O5−O6 distance of 2.5 Å calculated for S 3 O is much larger than that observed in the XFEL structures.…”

Jahn‐Teller Effects in a Vanadate‐Stabilized Manganese‐Oxo Cubane Water Oxidation Catalyst

“…In passing we note that the JT effect is also intensely discussed in relation to the oxygen evolving catalyst, see, e. g., Refs. [12,14,[30][31][32][33].…”

The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

“…[32][33][34][35][36][37] In addition to this water uptake (denoted by a W superscript; Scheme 2), in each S state the cluster can attain at least two different conformations. 18,[38][39][40][41]56 This is best documented for the S 2 state, where the two conformations give rise to the low spin (LS) S 2 g ¼ 2 multiline and the broad high-spin (HS) g ¼ 4-6 EPR signals, respectively.…”