New Water Oxidation Mechanism in Photosystem II Resolves Major Experimental Controversies

Light-driven oxygen formation in photosystem II protein is a fundamental process that sustains our biosphere. The research by advanced physical techniques has delivered new insights on the structure and function of the Mn₄CaO₅ cluster. However, discrepancies in experimental observations and computational models persist, impeding the understanding of O-O bond formation and the role of the protein environment in the process. Here, we show that i) assignment of the OEC unique oxygen O3 ligated by histidine (His337) via dynamic H-bond as a slow exchanging substrate and ii) its coupling with O6 oxygen generated at Mn1 in the S₂ to S₃ transition-giving an O─O bond formation mechanism most consistent with all currently available experimental data. We propose a mechanism by which the protein environment can steer the O─O bond formation by charge control via H-bonding and open coordination of Mn1. Obtained O3-O6 peroxide is at lower energy than peroxides in the most studied O5─O6 bond formation pathway. His337 appears to be similar to distal His in globins used for management of the O₂ and H₂O₂ intermediates. This new mechanism breaks the prior impasse and will undoubtedly invigorate future detailed studies uncovering further details.