Very recently, highly efficient biomimetic models of the mononuclear copper enzyme galactose oxidase were synthesized which are able to reproduce the structural, spectroscopic, and functional properties of the native system exceptionally well. We have characterized an inactive and an active form of one of these biomimetic compounds using unrestricted dynamical density functional calculations. The peculiar nonsquare planar O N -coordination geometry of the copper ion in the catalytically 2 2
Ε½
. inactive EPR-active form induces a complex energy-level diagram that cannot be related to crystal-field models: The highest occupied orbitals are located on the -system of the aromatic ligands and are essentially spin-paired while the unpaired electron is localized mainly in a lower-lying d 2 2 orbital of the copper. Using ab initio molecular x yy dynamics simulations, we determined for the first time the structure of the active form complexed with a substrate analog. Our calculations reveal that upon substrate binding one of the phenolate ligands is pushed away from the copper center into an axial position and the electronic structure rearranges to an unusual antiferromagnetic diradical state. As in the inactive form, the unpaired β£-spin density is located in the copper d 2 2
x yy orbital. The unpaired β€-spin density, instead, is localized on the axial ligand in agreement with the ligand-based radical mechanism that has been proposed for galactose oxidase.