Electronic structure studies of oxomolybdenum tetrathiolate complexes: Origin of reduction potential differences and relationship to cysteine-molybdenum bonding in sulfite oxidase

Electronic absorption, magnetic circular dichroism, and resonance Raman spe ctroscopies have been used to determine the nature of oxomolybdenum-thiolat e bonding in (PPh4)[MoO(SPh)(4)] (SPh = phenylthiolate) and (HNEt3) [MoO(SP h-PhS)(2)] (SPh-PhS = biphenyl-2,2'-dithiolate). These compounds, like all oxomolybdenum tetraarylthiolate complexes previously reported, display an i ntense low-energy charge-transfer feature that we have now shown to be comp rised of multiple S --> Mo d(xy) transitions. The integrated intensity of t his low-energy band in [MoO(SPh)(4)](-) is approximately twice that of [MoO (SPh-PhS)(2)](-), implying a greater covalent reduction of the effective nu clear charge localized on the molybdenum ion of the former and a concomitan t negative shift in the Mo(V)/Mo(TV) reduction potential brought about by t he differential S - Mo d(xy) charge donation. However, this is not observed experimentally; the Mo(V)/Mo(IV) reduction potential of [MoO(SPh)(4)](-) i s similar to 120 mV more positive than that of [MoO(SPh-PhS)(2)](-) (-783 v s -900 mV). Additional electronic factors as well as structural reorganizat ional factors appear to play a role in these reduction potential difference s. Density functional theory calculations indicate that the electronic cont ribution results from a greater sigma -mediated charge donation to unfilled higher energy molybdenum acceptor orbitals, and this is reflected in the i ncreased energies of the [MoO(SPh-PhS)(2)](-) ligand-to-metal charge-transf er transitions relative to those of [MoO(SPh)(4)](-). The degree of S-Mo d( xy) covalency is a function of the O drop Mo-S-C dihedral angle, with incre asing charge donation to Mo d(xy) and increasing charge-transfer intensity occurring as the dihedral angle decreases from 90 to 0 degrees. These resul ts have implications regarding the role of the coordinated cysteine residue in sulfite oxidase. Although the O drop Mo-S-C dihedral angles are either similar to 59 or similar to 121 degrees in these oxomolybdenum tetraarylthi olate complexes, the crystal structure of the enzyme reveals an O drop Mo-S -Cys-C angle of similar to 90 degrees. Thus, a significant reduction in S-C ys-Mo d(xy) covalency is anticipated in sulfite oxidase. This is postulated to preclude the direct involvement of coordinated cysteine in coupling the active site into efficient superexchange pathways for electron transfer, p rovided the O drop Mo-S-Cys-C angle is not dynamic during the course of cat alysis. Therefore, we propose that a primary role for coordinated cysteine in sulfite oxidase is to statically poise the reduced molybdenum center at more negative reduction potentials in order to thermodynamically facilitate electron transfer from Mo(IV) to the endogenous b-type heme.