Reversible Structural Isomerization of Nature's Water Oxidation Prior to O-O Bond Formation

Photosynthetic water oxidation is catalyzed by a manganese-calcium oxide cluster, which experiences five S-states during a light-driven reaction cycle. The unique distorted chairlike geometry of the Mn4CaO5(6) cluster shows structural flexibility that has been frequently proposed to involve open and closedcubane forms from the S-1 to S-3 states. The isomers are interconvertible in the S-1 and S-2 states, while in the S-3 state, the open-cubane structure is observed to dominate in Thermosynechococcus elongatus (cyanobacteria) samples. In this work, using density functional theory calculations, we go beyond the S3+Yz state to the (S3Yz center dot)-Y-n -> S4+Yz step, and report for the first time that the reversible isomerism, which is suppressed in the S3+Yz state, is fully recovered in the ensuing (S3Yz center dot)-Y-n state due to the proton release from a manganese-bound water ligand. The altered coordination strength of the manganese-ligand facilitates formation of the closed-cubane form, in a dynamic equilibrium with the open-cubane form. This tautomerism immediately preceding dioxygen formation may constitute the rate limiting step for O-2 formation, and exert a significant influence on the water oxidation mechanism in photosystem II.

Automated summary

Photosynthetic water oxidation, catalyzed by a manganese-calcium oxide cluster, undergoes five different states during the reaction cycle. The unique geometry of the cluster allows for structural flexibility and interconversion between different forms at different states. This study reveals that a reversible isomerism, suppressed in one state, is fully recovered in the following state due to the release of a proton from a water ligand bound to the manganese. The altered coordination strength of the manganese-ligand facilitates a shift in the cluster's structure, affecting the water oxidation mechanism.