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, 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 Mn4CaO5 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” MnIII 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. © 2021 The Authors. Angewandte Chemie International Edition published by Wiley-VCH Gmb

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, 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 Mn4CaO5 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” MnIII 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

Arrested Substrate Binding Resolves Catalytic Intermediates in Higher‐Plant Water Oxidation

Among the intermediate catalytic steps of the water‐oxidizing Mn4CaO5 cluster of photosystem II (PSII), the final metastable S3 state is critically important because it binds one substrate and precedes O2 evolution. Herein, we combine X‐ and Q‐band EPR experiments on native and methanol‐treated PSII of Spinacia oleracea and show that methanol‐treated PSII preparations of the S3 state correspond to a previously uncharacterized high‐spin (S=6) species. This is confirmed as a major component also in intact photosynthetic membranes, coexisting with the previously known intermediate‐spin conformation (S=3). The high‐spin intermediate is assigned to a water‐unbound form, with a MnIV3 subunit interacting ferromagnetically via anisotropic exchange with a coordinatively unsaturated MnIV ion. These results resolve and define the structural heterogeneity of the S3 state, providing constraints on the S3 to S4 transition, on substrate identity and delivery pathways, and on the mechanism of O−O bond formation

Coordination behavior of 3-Ethoxycarbonyltetronic acid towards Cu(II) and Co(II) metal ions

Tetronic acids, 4-hydroxy-5H-furan-2-ones, constitute a class of heterocyclic compounds with potent biological and pharmacological activity. The , -tricarbonyl moiety plays an integral role in biological systems and forms a variety of metal complexes. In this report, we present the complexation reactions of 3-ethoxycarbonyl tetronic acids with acetates and chlorides of Cu(II) and Co(II). These complexes have been studied by means of EPR spectroscopy and magnetic susceptibility measurements. From the obtained results, a preliminary complexation mode of the ligand is proposed

Proton Translocation via Tautomerization of Asn298 During the S-2-S-3 State Transition in the Oxygen-Evolving Complex of Photosystem II

In biological water oxidation, a redox-active tyrosine residue (D1-Tyr161 or Y-Z) mediates electron transfer between the Mn4CaO5 cluster of the driving the cluster through progressively higher oxidation states S-i (i = 0-4). In contrast to lower S-states (S-0, S-1), in higher S-states (S-2, S-3) of the Mn4CaO5 cluster, Yz cannot be oxidized at cryogenic temperatures due to the accumulation of positive charge in the S-1 -> S-2 transition. However, oxidation of Y-Z by illumination of S-2 at 77-190 K followed by rapid freezing and charge recombination between Yz and the plastoquinone radical Q(A)(center dot-) allows trapping of an S-2 variant, the so-called S-2(trapped) state (S-2(t)), that is capable of forming Y-z(center dot) at cryogenic temperature. To identify the differences between the S-2 and S-2(t) states, we used the (S2Yz center dot)-Y-t intermediate as a probe for the S-2(t) state and followed the (S2Yz center dot)-Y-t/Q(A)(center dot-) recombination kinetics at 10 K using time-resolved electron paramagnetic resonance spectroscopy in H2O and D2O. The results show that while (S2Yz center dot)-Y-t/Q(A)(center dot-) recombination can be described as pure electron transfer occurring in the Marcus inverted region, the S-2(t) -> S-2 reversion depends on proton rearrangement and exhibits a strong kinetic isotope effect. This suggests that Y-Z oxidation in the 521 state is facilitated by favorable proton redistribution in the vicinity of Y-Z, most likely within the hydrogen-bonded Y-Z-His190-Asn298 triad. Computational models show that tautomerization of Asn298 to its imidic acid form enables proton translocation to an adjacent asparagine-rich cavity of water molecules that functions as a proton reservoir and can further participate in proton egress to the lumen

Dielectric studies of a bioactive tetramic acid and its complexes with Cu(II) and Co(II)

The 3-acyl tetramic acids constitute a growing class of natural products displaying a range of biological activities. The β,β′ tricarbonyl moiety present in the 3-acyl tetramic acid provides a suitable site for bidentate complexation to a metal, which increases the biological activity. For the dielectric study of N-acetyl-3-butanoyl tetramic acid and a series of its complexes with Cu(II) and Co(II) in symmetric and asymmetric forms, we used the Thermally Stimulated Depolarization Currents (TSDC) technique. The drastic decrease of the intensity of the TSDC peaks of the symmetric and asymmetric complexes, compared to the above mentioned ligand, suggested that the polarizability of the side groups is considerably reduced. This result enhances the proposed complexation mode of the ligand through oxygen next to carbons 3 and 4 of the 5-member ring

Electronic properties of the S = 5/2 Mn(II) complexes [Mn{PhC(O)NP(O)PPh₂}(N,N)(NO₃)], (N,N) = phenanthroline, neocuproine, 2,2′-bipyridine

The synthesis, as well as the structural and electronic properties of the [Mn(O,O)(N,N)(NO3)] complexes, (O,O) = {PhC(O)NP(O)PPh2}−, (N,N) = phenanthroline (1), neocuproine (2) and 2,2′-bipyridine (3) is reported. The three complexes were structurally characterized by X-ray crystallography, and complexes 1 and 2 were shown to be closer to octahedral, whereas 3 to trigonal prismatic. The zero-field splitting parameters of these S = 5/2 systems were determined by X- and Q-band EPR spectroscopy, revealing a small but significant difference in the magnitude of |D| for complex 3 (0.18 cm−1) compared to those of 1 and 2 (0.14 and 0.12 cm−1, respectively). These differences are attributed to the structural and electronic properties of complexes 1–3. The latter were probed by DFT calculations, which showed different DSOC contributions among the three complexes