O2 evolution and recovery of the water-oxidizing enzyme

Abstract

In photosystem II, light-induced water oxidation occurs at the Mn₄CaO₅ cluster. Here we demonstrate proton releases, dioxygen formation, and substrate water incorporation in response to Mn₄CaO₅ oxidation in the protein environment, using a quantum mechanical/molecular mechanical approach and molecular dynamics simulations. In S₂, H₂O at the W1 site forms a low-barrier H-bond with D1-Asp61. In the S₂-to-S₃ transition, oxidation of O_W1H^- to O_W1^•-, concerted proton transfer from O_W1H^- to D1-Asp61, and binding of a water molecule W_n-W1 at O_W1^•- are observed. In S₄, W _n_-W1 facilitates oxo-oxyl radical coupling between O_W1^•- and corner μ-oxo O4. Deprotonation via D1-Asp61 leads to formation of O_W1=O4. As O_W1=O4 moves away from Mn, H₂O at W539 is incorporated into the vacant O4 site of the O₂-evolved Mn₄CaO₄ cluster, forming a μ-oxo bridge (Mn3-O_W539-Mn4) in an exergonic process. Simultaneously, W_n-W1 is incorporated as W1, recovering the Mn₄CaO₅ cluster.