Electronic structures of exchange coupled trigonal trimeric Cu(II) complexes: Spin frustration, antisymmetric exchange, pseudo-A terms, and their relation to O2 activation in the multicopper oxidases

Exchange coupled trinuclear Cu(II) clusters are of great importance in magnetic materials as well as in key steps of biological catalysis. However, the physical origins of the unique magnetic and spectroscopic features have been elusive and detailed descriptions of their electronic structures have been limited. In this review, we review our recent spectroscopic studies on structurally well-defined trinuclear Cu(II) model complexes with distinct Cu–O bridged structures that represent the 4e− reduced, native intermediate in the catalytic reactivity of the multicopper oxidases. Our studies mainly based on electron paramagnetic resonance (EPR) and magnetic circular dichroism (MCD) experiments provide new insights into the metal–ligand bonding interactions in the ground and excited states of the exchange coupled Cu(II) trimers: (1) the spin frustrated ground state of an antiferromagnetically coupled Cu(II) trimer undergoes zero-field splitting into two doublet states via a first-order spin–orbit coupling effect, termed antisymmetric exchange, that requires effective ground-to-excited state superexchange interactions, and (2) the ligand-to-metal charge transfer excited states undergo coupling interactions via either metal- or ligand-based, single-centered spin–orbit coupling mechanisms. The former is reflected in extremely unusual ground state EPR spectral features, while the latter is manifested in the MCD spectrum of the excited states as a set of two field- and temperature-dependent MCD C-terms with opposite signs. This MCD feature, called a pseudo-A term, has allowed differentiation of geometrically distinct Cu–O chromophores of the two model complexes and determination of the structure of the native intermediate in the reduction of O2 to H2O by the multicopper oxidases. The fundamental descriptions of the electronic structures of exchange coupled Cu(II) trimers implicate their significant roles in the catalytic reductive cleavage of OO bonds in biology and in the physical properties of magnetic materials.