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

Abstract

Electronic absorption, magnetic circular dichroism, and resonance Raman spectroscopies have been used to determine the nature of oxomolybdenum-thiolate bonding in (PPh4)[MoO(SPh)4] (SPh = phenylthiolate) and (HNEt3)[MoO(SPh-PhS)2] (SPh-PhS = biphenyl-2,2'-dithiolate). These compounds, like all oxomolybdenum tetraarylthiolate complexes previously reported, display an intense low-energy charge-transfer feature that we have now shown to be comprised of multiple S-->Mo dxy transitions. The integrated intensity of this low-energy band in [MoO(SPh)4]- is approximately twice that of [MoO(SPh-PhS)2]-, implying a greater covalent reduction of the effective nuclear charge localized on the molybdenum ion of the former and a concomitant negative shift in the Mo(V)/Mo(IV) reduction potential brought about by the differential S-->Mo dxy charge donation. However, this is not observed experimentally; the Mo(V)/Mo(IV) reduction potential of [MoO(SPh)4]- is approximately 120 mV more positive than that of [MoO(SPh-PhS)2]- (-783 vs -900 mV). Additional electronic factors as well as structural reorganizational factors appear to play a role in these reduction potential differences. Density functional theory calculations indicate that the electronic contribution results from a greater sigma-mediated charge donation to unfilled higher energy molybdenum acceptor orbitals, and this is reflected in the increased energies of the [MoO(SPh-PhS)2]- ligand-to-metal charge-transfer transitions relative to those of [MoO(SPh)4]-. The degree of S-Mo dxy covalency is a function of the O identical to Mo-S-C dihedral angle, with increasing charge donation to Mo dxy and increasing charge-transfer intensity occurring as the dihedral angle decreases from 90 to 0 degree. These results have implications regarding the role of the coordinated cysteine residue in sulfite oxidase. Although the O identical to Mo-S-C dihedral angles are either approximately 59 or approximately 121 degrees in these oxomolybdenum tetraarylthiolate complexes, the crystal structure of the enzyme reveals an O identical to Mo-SCys-C angle of approximately 90 degrees. Thus, a significant reduction in SCys-Mo dxy 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, provided the O identical to Mo-SCys-C angle is not dynamic during the course of catalysis. 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.