Electronic Structure Studies of Oxomolybdenum Tetrathiolate Complexes:  Origin of Reduction Potential Differences and Relationship to Cysteine−Molybdenum Bonding in Sulfite Oxidase

• Published in: Inorganic chemistry 2000-12, Vol.39 (25), p.5697-5706
• Main Authors: McNaughton, Rebecca L, Tipton, A. Alex, Rubie, Nick D, Conry, Rebecca R, Kirk, Martin L
• Format: Article
• Language: English
• Subjects: Binding Sites; Circular Dichroism; Cysteine - chemistry; Kinetics; Models, Molecular; Molecular Conformation; Molybdenum - chemistry; Organometallic Compounds - chemistry; Oxidation-Reduction; Oxidoreductases Acting on Sulfur Group Donors - chemistry; Oxidoreductases Acting on Sulfur Group Donors - metabolism; Protein Conformation; Spectrophotometry; Spectrum Analysis, Raman; Sulfhydryl Compounds - chemistry
• ISSN: 0020-1669; 1520-510X
• DOI: 10.1021/ic0003729

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 d xy 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 d xy charge donation. However, this is not observed experimentally; the Mo(V)/Mo(IV) reduction potential of [MoO(SPh)4]- is ∼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 σ-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 d xy covalency is a function of the O⋮MoSC dihedral angle, with increasing charge donation to Mo d xy and increasing charge-transfer intensity occurring as the dihedral angle decreases from 90 to 0°. These results have implications regarding the role of the coordinated cysteine residue in sulfite oxidase. Although the O⋮MoSC dihedral angles are either ∼59 or ∼121° in these oxomolybdenum tetraarylthiolate complexes, the crystal structure of the enzyme reveals an O⋮Mo−SCys−C angle of ∼90°. Thus, a significant reduction in SCys−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, provided the O⋮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