In this report we combine broken symmetry density functional calculations and electron paramagnetic resonance analysis to obtain the electronic structure of the penultimate S3 state of Nature’s water oxidising 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 oxidising complex are used to provide a unique low energy pathway. The pathway is facilitated via formation and stabilisation of the [O2]3- ion. This ion is formed between ligated deprotonated substrate waters, O5 and O6, and is stabilised by antiferromagnetic interaction with the Mn ions of the complex. Combining computational, crystallographic and spectroscopic data we show that an equilibrium exists between an O5 oxo and O6 hydroxo form with an S=3 spin state and a deprotonated O6 form containing a two-centre 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. Analysis of the most recent X-ray emission spectroscopy (XES) 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 i.e. [O5O6]3-. Progression of this form to the two-electron oxidised peroxo and three-electron oxidised superoxo forms, leading eventually to the evolution of triplet O2, is proposed to be the pathway Nature adopts to oxidise water. The study reveals the key electronic, magnetic and structural design features of Nature’s catalyst which facilitates water oxidation to O2 under ambient conditions.
Correction of typographical errors in previous version
How Nature makes O2: an electronic level mechanism for water oxidation in photosynthesis.