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

Abstract

The S₃ state is currently the last observable intermediate prior to O-O bond formation at the oxygen-evolving complex (OEC) of Photosystem II, and its electronic structure has been assigned to a homovalent Mn^IV₄ core with an S = 3 ground state. While structural interpretations based on the EPR spectroscopic features of the S₃ state provide valuable mechanistic insight, corresponding synthetic and spectroscopic studies on tetranuclear complexes mirroring the Mn oxidation states of the S₃ state remain rare. Herein, we report the synthesis and characterization by XAS and multifrequency EPR spectroscopy of a Mn^IV₄O₄ cuboidal complex as a spectroscopic model of the S₃ state. Results show that this Mn^IV₄O₄ complex has an S = 3 ground state with isotropic ⁵⁵Mn hyperfine coupling constants of -75, -88, -91, and 66 MHz. These parameters are consistent with an αααβ spin topology approaching the trimer-monomer magnetic coupling model of pseudo-octahedral Mn^IV centers. Importantly, the spin ground state changes from S = 1/2 to S = 3 as the OEC is oxidized from the S₂ state to the S₃ state. This same spin state change is observed following oxidation of the previously reported Mn^IIIMn^IV₃O₄ cuboidal complex to the Mn^IV₄O₄ complex described here. This sets a synthetic precedent for the observed low-spin to high-spin conversion in the OEC.

Figure 1.

a) Proposed isomers S₃^A and S₃^B of the inorganic CaMn₄O₅(OH) core of the S₃ state of the OEC. b) Representative examples of Mn^IV₄ complexes and their corresponding spin ground states.

Figure 2.

Mn K-edge XAS spectra for complexes 2 (black lines) and 3 (red dotted lines). a) Normalized XANES data, b) k³-weighted EXAFS data, and c) Fourier transforms of k³-weighted EXAFS data.

Figure 3.

D-band EPR spectrum of complex 3 collected at 1.6 K. Spectral data are shown in black and the simulated spectrum is represented by the dashed red line and other colored traces. The simulated Mn(II) contribution is shown in light blue and the m_S transitions that contribute to the complex 3 simulation are shown in blue, purple, and orange. Simulation parameters: S = 3, g = 1.97, D = 0.4 cm⁻¹, E/D = 0.1. (Inset) Electron-spin nutation curves of complex 3 (blue) collected at 7 T and BDPA (black).

Figure 4.

Parallel mode X-band CW-EPR of complex 3. Spectral data are shown in black and the simulated spectrum is represented by the dashed red line. Simulation parameters: S = 3, g = 1.97, D = 0.4 cm⁻¹, E/D = 0.1.

Figure 5.

(Left) EPR spectrum of 3 showing the field positions (*) where EDNMR spectra were collected. (Right) Field dependent EDNMR of 3. Experimental data are shown in black traces. Spectral simulations are shown in the colored traces. The simulated hyperfine values are listed in Table 1.

Scheme 1.

Synthesis of complexes 1~3 studied in this work.