High-spin Mn-oxo complexes and their relevance to the oxygen-evolving complex within photosystem II

Abstract

The structural and electronic properties of a series of manganese complexes with terminal oxido ligands are described. The complexes span three different oxidation states at the manganese center (III-V), have similar molecular structures, and contain intramolecular hydrogen-bonding networks surrounding the Mn-oxo unit. Structural studies using X-ray absorption methods indicated that each complex is mononuclear and that oxidation occurs at the manganese centers, which is also supported by electron paramagnetic resonance (EPR) studies. This gives a high-spin Mn(V)-oxo complex and not a Mn(IV)-oxy radical as the most oxidized species. In addition, the EPR findings demonstrated that the Fermi contact term could experimentally substantiate the oxidation states at the manganese centers and the covalency in the metal-ligand bonding. Oxygen-17-labeled samples were used to determine spin density within the Mn-oxo unit, with the greatest delocalization occurring within the Mn(V)-oxo species (0.45 spins on the oxido ligand). The experimental results coupled with density functional theory studies show a large amount of covalency within the Mn-oxo bonds. Finally, these results are examined within the context of possible mechanisms associated with photosynthetic water oxidation; specifically, the possible identity of the proposed high valent Mn-oxo species that is postulated to form during turnover is discussed.

Keywords: inorganic chemistry; metal–oxo complexes; oxygen-evolving complex; photosynthesis; water oxidation.

Fig. 1.

(A–D) Structures of the OEC cluster illustrating the hydrogen-bonding network (A) (purple spheres, Mn; light blue spheres, Ca²⁺; red spheres, oxido/hydroxo ligands; blue sphere, nitrogen; white spheres, water), the nucleophilic mechanism for O–O bond formation (B), the radical coupling mechanism for O–O bond formation (C), and the Mn–oxo complexes used in this study (D). The structure in A is adapted from Protein Data Bank ID 3BZ1.

Fig. 2.

Q- and X-band parallel-mode EPR spectra of the Mn^III–oxo complex, 10 mM in 1:1 dimethyformamide (DMF):tetrahydrofuran (THF). The colored traces are experimental data and the black traces are simulation of the corresponding spectra using the parameters given in Table 2. Inset shows the broadening of a hyperfine line at 68 mT due to ¹⁷O enrichment. Experimental conditions: temperature 10 K; frequency 33.906 GHz (Q), 9.298 GHz (X); and power 5 mW (Q), 20 mW (X).

Fig. 3.

S- and X-band perpendicular-mode EPR spectra of the Mn^IV–oxo complex, 30 mM in 1:1 DMF:THF. The black lines are simulation of the corresponding spectra using the parameters given in Table 2. Experimental conditions: temperature 12 K; frequency 3.500 GHz (S), 9.642 GHz (X); and power 0.03 mW (S), 0.20 mW (X). A minor impurity occurs near g = 2.00 in both spectra.

Fig. 4.

X-band parallel-mode EPR spectra of the Mn^V–oxo complex, 25 mM in 1:1 DMF:THF. The red traces are data and the black traces are simulations. Inset shows the broadening of a region of hyperfine lines due to ¹⁷O enrichment. Experimental conditions: temperature 11 K, frequency 9.332 GHz, and power 20 mW. The simulation parameters are given in Table 2.

Fig. 5.

Relaxed potential energy scans of the Mn^V–oxo (S = 1) ground state (lower curve) and the Mn^IV–oxyl (S = 1) broken symmetry configuration (upper curve) along the Mn–O coordinate. The solid curves are parabolic fits of the DFT-generated points obtained from B3LYP/6-311G calculations. Insets show total spin density contour plots for the two states.