How Nature Makes O(2): an Electronic Level Mechanism for Water Oxidation in Photosynthesis

[Image: see text] In this paper, we combine broken symmetry density functional calculations and electron paramagnetic resonance analysis to obtain the electronic structure of the penultimate S(3) state of nature’s water-oxidizing complex and determine the electronic pathway of O–O bond formation. Analysis of the electronic structure changes along the reaction path shows that two spin crossovers, facilitated by the geometry and magnetism of the water-oxidizing complex, are used to provide a unique low-energy pathway. The pathway is facilitated via the formation and stabilization of the [O(2)](3–) ion. This ion is formed between ligated deprotonated substrate waters, O5 and O6, and is stabilized by antiferromagnetic interaction with the Mn ions of the complex. Combining the computational, crystallographic, and spectroscopic data, we show that an equilibrium exists between the O5 oxo and O6 hydroxo forms with an S = 3 spin state and a deprotonated O6 form containing a two-center one-electron bond in [O5O6](3–) which we identify as the form detected using crystallography. This form corresponds to an S = 6 spin state which we demonstrate gives rise to a low-intensity EPR spectrum compared with the accompanying S = 3 state, making its detection via EPR difficult and overshadowed by the S = 3 form. Simulations using 70% of the S = 6 component give rise to a superior fit to the experimental W-band EPR spectral envelope compared with an S = 3 only form. Analyses of the most recent X-ray emission spectroscopy first moment changes for solution and time-resolved crystal data are also shown to support the model. The computational, crystallographic, and spectroscopic data are shown to coalesce to the same picture of a predominant S = 6 species containing the first one-electron oxidation product of two water molecules, that is, [O5O6](3–). Progression of this form to the two-electron-oxidized peroxo and three-electron-oxidized superoxo forms, leading eventually to the evolution of triplet O(2), is proposed to be the pathway nature adopts to oxidize water. The study reveals the key electronic, magnetic, and structural design features of nature’s catalyst which facilitates water oxidation to O(2) under ambient conditions.