O(2) evolution and recovery of the water-oxidizing enzyme

In photosystem II, light-induced water oxidation occurs at the Mn(4)CaO(5) cluster. Here we demonstrate proton releases, dioxygen formation, and substrate water incorporation in response to Mn(4)CaO(5) oxidation in the protein environment, using a quantum mechanical/molecular mechanical approach and molecular dynamics simulations. In S(2), H(2)O at the W1 site forms a low-barrier H-bond with D1-Asp61. In the S(2)-to-S(3) transition, oxidation of O(W1)H(–) to O(W1)(•–), concerted proton transfer from O(W1)H(–) to D1-Asp61, and binding of a water molecule W(n-W1) at O(W1)(•–) are observed. In S(4), 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, H(2)O at W539 is incorporated into the vacant O4 site of the O(2)-evolved Mn(4)CaO(4) cluster, forming a μ-oxo bridge (Mn3–O(W539)–Mn4) in an exergonic process. Simultaneously, W(n-W1) is incorporated as W1, recovering the Mn(4)CaO(5) cluster.