Various mechanisms have been proposed for the initial O2 attack in intradiol dioxygenases based on different electronic descriptions of the enzyme-substrate (ES) complex. We have examined the geometric and electronic structure of the high-spin ferric ES complex of protocatechuate 3,4-dioxygenase (3,4-PCD) with UV/visible absorption, circular dichroism (CD), magnetic CD (MCD), and variable-temperature variable-field (VTVH) MCD spectroscopies. The experimental data were coupled with DFT and INDO/S-CI calculations, and an experimentally calibrated bonding description was obtained. The broad absorption spectrum for the ES complex in the 6000-31000 cm-1 region was resolved into at least five individual transitions, assigned as ligand-to-metal charge transfer (LMCT) from the protocatechuate (PCA) substrate and Tyr408. From our DFT calculations, all five LMCT transitions originate from the PCA and Tyr πop orbitals to the ferric dπ orbitals. The strong π covalent donor interactions dominate the bonding in the ES complex. Using hypothetical Ga3+-catecholate/semiquinone complexes as references, 3,4-PCD-PCA was found to be best described as a highly covalent Fe 3+-catecholate complex. The covalency is distributed unevenly among the four PCA valence orbitals, with the strongest interaction between the πop-sym and Fe dxz orbitals. This strong π interaction, as reflected in the lowest energy PCA-to-Fe3+ LMCT transition, is responsible for substrate activation for the O2 reaction of intradiol dioxygenases. This involves a multi-electron-transfer (one β and two α) mechanism, with Fe3+ acting as a buffer for the spin-forbidden two-electron redox process between PCA and O2 in the formation of the peroxy-bridged ESO2 intermediate. The Fe ligand field overcomes the spin-forbidden nature of the triplet O2 reaction, which potentially results in an intermediate spin state (S = 3/2) on the Fe3+ center which is stabilized by a change in coordination along the reaction coordinate.