New Water Oxidation Mechanism in Photosystem II Resolves Major Experimental Controversies

ABSTRACT

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 Mn ₄ CaO ₅ 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 S ₂ to S ₃ 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 O ₂ and H ₂ O ₂ intermediates. This new mechanism breaks the prior impasse and will undoubtedly invigorate future detailed studies uncovering further details.