Dioxygen Binding to Deoxyhemocyanin: Electronic Structure and Mechanism of the Spin-Forbidden Two-Electron Reduction of O2

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Abstract
Spectroscopically calibrated DFT is used to investigate the reaction coordinate of O2 binding to Hemocyanin (Hc). A reaction path is calculated in which O2 approaches the binuclear copper site with increasing metal−ligand overlap, which switches the coordination mode from end-on η1-η1, to μ-η1:η2, then to butterfly, and finally to the planar [Cu2(μ-η2:η2O2)] structure. Analysis of the electronic structures during O2 binding reveals that simultaneous two-electron transfer (ET) takes place. At early stages of O2 binding the energy difference between the triplet and the singlet state is reduced by charge transfer (CT), which delocalizes the unpaired electrons and thus lowers the exchange stabilization onto the separated copper centers. The electron spins on the copper(II) ions are initially ferromagnetically coupled due to close to orthogonal magnetic orbital pathways through the dioxygen bridging ligand, and a change in the structure of the Cu2O2 core turns on the superexchange coupling between the coppers. This favors the singlet state over the triplet state enabling intersystem crossing. Comparison with mononuclear model complexes indicates that the protein matrix holds the two copper(I) centers in close proximity, which enthalpically and entropically favors O2 binding due to destabilization of the reduced binuclear site. This also allows regulation of the enthalpy by the change of the Cu−Cu distance in deoxyHc, which provides an explanation for the O2 binding cooperativity in Hc. These results are compared to our earlier studies of Hemerythrin (Hr) and a common theme emerges where the spin forbiddeness of O2 binding is overcome through delocalization of unpaired electrons onto the metal centers and the superexchange coupling of the metal centers via a ligand bridge.