Studies on the electronic structure of the two physiologically relevant forms of hemerythrin (Hr), i.e., deoxyHr (possessing a hydroxo-bridged diferrous site) and oxyHr (having an ore-bridged diferric site with a terminal hydroperoxide), are presented and discussed. SQUID magnetic susceptibility data for deoxyHr confirm that the two ferrous ions are weakly antiferromagnetically coupled, J = -14(2) cm(-1) (H= -2JS(1). S-2), indicating that at 300 K the entire manifold of ground-state spin sublevels is available for the reaction with O-2. From density functional calculations on deoxyHr, evaluated on the basis of experimental data, the redox active orbital on the five-coordinate iron (Fe2) is favorably oriented for a rr-bonding interaction with O-2 approaching along the open coordination site of that center, and reorientation of the redox active orbital on the six-coordinate iron (Fel) for electron transfer to O-2 through superexchange with Fe2 is energetically accessible. Analysis of existing spectroscopic data for oxyHr using Heller's time-dependent theory leads to the proposal that the peculiar behavior of the UV resonance Raman excitation profile for the symmetric Fe-O-Fe stretching mode v(Fe-O) to peak with fairly minor absorption features arises from interference effects between oxo to-Fe charge-transfer excited states. From density functional calculations on oxyHr and related structures the low frequency of the Fe-oxo stretch is ascribed to the hydrogen bond between the hydroperoxide and the bridging oxide, whereas the small (\J\ value appears to be due primarily to the strong hydroperoxide --> Fe2 pi-donor interaction that reduces Fel --> Fe2 electron delocalization.