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

Abstract

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, S₂ . 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 Mn₄ CaO₅ cluster in the resting (dark-stable) S₁ 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 S₁ state. This unique isomerism in the resting state is shown to be the electronic origin of valence isomerism in the S₂ state, establishing a functional role of orientational Jahn-Teller isomerism unprecedented in biological or artificial catalysis.

Keywords: EPR spectroscopy; bioinorganic chemistry; computational chemistry; electronic structure; photosynthesis.

Figure 1

a) Structure of the oxygen‐evolving complex suggested by crystallography (PDB ID: 5B66). ^[13] b) The S‐state cycle of the OEC, illustrating the light‐induced one‐electron oxidation steps coupled to proton release, the uptake of substrate water molecules, and O₂ evolution. Electron transfer from the OEC to the P680 radical cation of the PSII reaction center is mediated by a redox‐active tyrosine (Tyr161 or Y_Z) giving rise to metalloradical S_iY_Z ^. intermediates. c) Spectroscopically consistent S₂ state valence isomers S₂ ^A and S₂ ^B, which gate progression to a high‐spin water‐unbound form of the S₃ state. ^[27] The orientation of Jahn–Teller elongation for the Mn^III ion in each S₂ isomer is indicated with green arrows.

Figure 2

a) Core geometries of S₁ models S₁ ^A and S₁ ^B, with selected optimized bond lengths shown for comparison and with indication of the Jahn–Teller axis orientations (in green). b) Canonical molecular orbitals with Mn^III ${\mathrm{d}}_{z^2}$ character, showing the distinct orientation of the Mn4 ${\mathrm{d}}_{z^2}$ orbital in each isomer.

Figure 3

a) Potential energy surface resulting from the quadratic E⊗e coupling for an idealized octahedral Mn^III ion with illustration of the two types of distortion (see also Figure S1). b) Schematic depiction of the partial potential energy trough cross‐section suggested to survive for the orientational Jahn–Teller S₁ isomers identified here with respect to configurations of the terminal Mn4(III) ion. Jahn–Teller elongation axes depicted with green arrows.

Figure 4

a) Orientation of principal axes of D _SOC for Mn^III ions in the S₁ ^A and S₁ ^B Jahn–Teller isomers, computed by multireference L‐CASCI calculations. b) Simulations of the two types of S₁ EPR signal. Left: Simulation of EPR signal at g _eff≈4.8 using S=1; acceptable combinations of D and E/D parameters are shown in Figure S5. Right: Simulation of the S₁ EPR signal centered at g _eff≈12, using S=3, D=6.67 cm⁻¹, E/D=0.048.

Figure 5

Left: Correlation of Mn1 (blue line) and Mn4 (orange line) Mulliken spin populations with the Mn1‐O5 distance for one‐electron oxidized S₁ models derived from constrained geometry optimizations. Right: Correspondence between S₁ and S₂ isomer structures, showing how orientational Jahn–Teller isomerism in the dark‐stable S₁ state of the OEC leads upon oxidation to distinct oxidation state distributions in the S₂ state. The scheme indicates known EPR signals of the two states and metalloradical S₁Y_Z ^. intermediates, ^[58] showing how the isomeric forms accommodate spectroscopic observations into one coherent structural interpretation.