O-O Bond Formation in Photosystem II Oxygen Evolving Complex

Abstract

Photosynthetic water oxidation is a fundamental process that sustains the biosphere. Light driven water oxidation is facilitated in Nature by the Oxygen Evolving Complex (OEC) - Mn4Ca cluster embedded in the photosystem II protein. During its function, the OEC cycles through five redox states termed S0-S4 after which, oxygen is evolved. Here, time-resolved x-ray emission spectroscopy (XES) was used to observe the process of oxygen formation in real time. These experiments reveal that the oxygen evolution step, initiated by three sequential laser flashes, is accompanied by rapid (within 50 μs) changes to the Mn Kβ XES spectrum. However, no oxidation of the Mn4Ca core above the all MnIV state was detected to precede O-O bond formation, and the observed changes were therefore assigned to O-O bond formation dynamics. Our mechanism proposes O-O bond formation occurs prior to the transfer of the final (4th) electron from the Mn4Ca cluster to the oxidized TyrZ. This model resolves the kinetic limitations associated with O-O bond formation, and suggests an evolutionary adaptation to avoid releasing of harmful peroxide species. Atomistic model for the S3 state reported by us [1, 2] is indistinguishable (within the resolution of XRD) from one of the recently reported by Shen and co-workers [3]. This S3-state model incorporates a MnIV=O fragment of radicaloid character and exhibits antiferromagnetic alignment with opposite spin orientations between two Mn centers and associated oxygens creating an opportunity for a low barrier to O-O bond formation. 1. Davis et al. 2015, arXiv:1506.08862 2. Jensen et al. J Phys. Chem. Letters, 2017, 8, 2584−2589. 3. Suga et al. Nature, 2017, 543(7643), 131-135.