Molecular Identification of a High-Spin Deprotonated Intermediate during the S2 to S3 Transition of Nature’s Water-Oxidizing Complex

The identity of a key intermediate in the S2 to S3 transition of nature’s water-oxidizing complex (WOC) in Photosystem 2 is presented. Broken-symmetry density functional theory (BS-DFT) calculations and Heisenberg–Dirac–van Vleck (HDvV) spin ladder calculations show that an S2 state open cubane model of the WOC containing a μ-hydroxo O4 changes from an S = 5/2 form to an S = 7/2, form upon deprotonation of W1. Combined with X-band electron paramagnetic resonance (EPR) spectral analysis, this indicates that the g = 4.1 EPR signal corresponds to an S = 5/2 form of the WOC with W1 present as a water ligand to Mn4, while the g = 4.8/4.9 form observed at high pH values corresponds to an S = 7/2 form, with W1 as a hydroxo ligand. The latter is also likely to represent the form needed to progress to S3 in the functioning enzyme.