Sulfur K-Edge XAS and DFT Studies on NiII Complexes with Oxidized Thiolate Ligands:  Implications for the Roles of Oxidized Thiolates in the Active Sites of Fe and Co Nitrile Hydratase

S K-edge X-ray absorption spectroscopy data on a series of NiII complexes with thiolate (RS-) and oxidized thiolate (RSO2 -) ligands are used to quantify Ni−S bond covalency and its change upon ligand oxidation. Analyses of these results using geometry-optimized density functional theory (DFT) calculations suggest that the Ni−S σ bonds do not weaken on ligand oxidation. Molecular orbital analysis indicates that these oxidized thiolate ligands use filled high-lying S−O π* orbitals for strong σ donation. However, the RSO2 - ligands are poor π donors, as the orbital required for π interaction is used in the S−O σ-bond formation. The oxidation of the thiolate reduces the repulsion between electrons in the filled Ni t2 orbital and the thiolate out-of-plane π-donor orbital leading to shorter Ni−S bond length relative to that of the thiolate donor. The insights obtained from these results are relevant to the active sites of Fe- and Co-type nitrile hydratases (Nhase) that also have oxidized thiolate ligands. DFT calculations on models of the active site indicate that whereas the oxidation of these thiolates has a major effect in the axial ligand-binding affinity of the Fe-type Nhase (where there is both σ and π donation from the S ligands), it has only a limited effect on the sixth-ligand-binding affinity of the Co-type Nhases (where there is only σ donation). These oxidized residues may also play a role in substrate binding and proton shuttling at the active site.