Tetranuclear [Mn^IIIMn₃^IVO₄] Complexes as Spectroscopic Models of the S₂ State of the Oxygen Evolving Complex in Photosystem II

Abstract

Despite extensive biochemical, spectroscopic, and computational studies, the mechanism of biological water oxidation by the Oxygen Evolving Complex (OEC) of Photosystem II remains a subject of significant debate. Mechanistic proposals are guided by the characterization of reaction intermediates such as the S2 state, which features two characteristic EPR signals at g = 2 and g = 4.1. Two nearly isoenergetic structural isomers have been proposed as the source of these distinct signals, but relevant structure−electronic structure studies remain rare. Herein, we report the synthesis, crystal structure, electrochemistry, XAS, magnetic susceptibility, variable temperature CW-EPR, and pulse EPR data for a series of [MnIIIMn3IVO4] cuboidal complexes as spectroscopic models of the S2 state of the OEC. Resembling the oxidation state and EPR spectra of the S2 state of the OEC, these model complexes show two EPR signals, a broad low field signal and a multiline signal, that are remarkably similar to the biological system. The effect of systematic changes in the nature of the bridging ligands on spectroscopy were studied. Results show that the electronic structure of tetranuclear Mn complexes is highly sensitive to even small geometric changes and the nature of the bridging ligands. Our model studies suggest that the spectroscopic properties of the OEC may also react very sensitively to small changes in structure; the effect of protonation state and other reorganization processes need to be carefully assessed.

S = 3 Ground State for a Tetranuclear MnIV4O4 Complex Mimicking the S3 State of the Oxygen-Evolving Complex

“…The diamidate-bridged cuboidal complex LMn III 2 Mn IV 2 O 4 (diam)(OAc) (1) was used as a precursor for the targeted Mn IV 4 O 4 complex (Scheme 1). 24 In propylene carbonate, the cyclic voltammogram of 1 shows a reversible oxidation to the previously characterized one electron oxidized Mn III Mn 3 IV O 4 complex (2) at −50 mV vs Fc/Fc + . 24 A second quasi-reversible Mn III Mn 3 IV /Mn IV 4 couple is observed at +780 mV vs Fc/Fc + ( Figure S3).…”

“…Despite significant efforts to prepare tetra-and pentanuclear complexes as models of the OEC, relevant complexes in terms of structure, redox state, spectroscopy, and reactivity are rare. [24][25][26][27][28][29][30][31][32][33][34][35][36][37][38] On the basis of EPR, MCD, and X-ray spectroscopic studies, the electronic structure of the S 3 state has been assigned to a homovalent Mn IV 4 core with an S = 3 spin ground state. 5,[39][40][41] Two structural isomers S 3 A (dimer-ofdimers) and S 3 B (trimer-monomer), both with S = 3 spin ground states, have been invoked for the S 3 state ( Figure 1a).…”

“…5,42 A similar structural isomerism has been proposed for the S 2 state. 24,43 Such proposed structural changes may lead to differences in the sign and magnitude of the magnetic exchange interactions (J ij ) between adjacent Mn centers, which in turn affect not only the spin ground state of the cluster but also the observed sign and magnitude of the projected 55 Mn hyperfine interactions (A i ). [43][44] The observed A i for Mn ions in the S 3 state have been accommodated with the calculated J ij for the S 3 A structure.…”

Molecular Vibrations of an Oxygen‐Evolving Complex and Its Synthetic Mimic

“…Molecular biomimetic models moved a step closer to PSII with the synthesis of asymmetric clusters, that is, once an external manganese, with respect to a cubane structure, was observed. Agapie and co‐workers made a fundamental contribution in this direction by extensively exploring synthetic model complexes that mimicked the native OEC cluster: the asymmetric Mn 3 CaO 4 cubane core of the OEC was indeed obtained in some synthetic complexes; over several years, this was further refined to be increasingly similar to the OEC, and a series of cuboidal Mn 4 complexes were recently reported as spectroscopic models of the S 2 state of the OEC . Mukherjee et al.…”

“…Agapie and co-workersm ade af undamentalc ontribution in this direction by extensively exploring synthetic model complexes that mimicked the native OEC cluster:t he asymmetric Mn 3 CaO 4 cubane core of the OEC was indeedo btained in some synthetic complexes; [16] over several years, this was further refined to be increasingly similar to the OEC, [17,18] and a serieso fc uboidal Mn 4 complexes were recently reported as spectroscopicm odelso ft he S 2 state of the OEC. [19] Mukherjee et al obtained asynthetic complex containing the CaMn IV 3 CaO 4 core, in whicho ne Ca ion was attached to the Mn 3 CaO 4 cubane. [20] Zhang et al synthesised the core cubane structure, Mn 3 CaO 4 ,l inked to ad angling Mn through one oxo bridge and structurally mimicked the full site of the OEC in PSII more closely.…”