Analysis of the iron K-edge X-ray absorption spectrum (XAS) of the "dark", inactive form of nitrile hydratase (NHdk) from Rhodococcus sp. R312 confirms a 1:1 stoichiometry of nitric oxide bound to low-spin iron(III). We also report XAS analyses of four iron complexes of the pentadentate ligands 2,3,13,14-tetramethyl-4,8,12-triaza-3,12-pentadecadiene-2, 14-dithiolate (L2-, also denoted as (S2N3)-N-Me2(Pr,Pr)(2-)) and 2,12-dimethyl-3,7,11-triaza-2,11-tridecadiene-1,13-dithiolate (L'(2-), also denoted as S2N3(Pr,Pr)(2-)): five-coordinate (FeL)-L-II' and FeL+ and low-spin six-coordinate FeL(N-3) and FeL(NO)(+) (cationic species an PF6- salts). The XAS of FeL(N-3) and FeL(NO)(+) closely mimic the spectra of butyrate-stabilized active nitrile hydratase (NHlt) and NHdk, respectively. The 1s --> 3d pre-edge peak is about twice as intense in five-coordinate FeL+ than for the remaining samples, suggesting that the iron in both NHlt and NHdk is six-coordinate. This peak and other edge features are 1 eV higher in energy for NHdk and FeL(NO)(+), consistent with a {FeNO}(6) electron count for both the enzyme and the model. Analysis of the EXAFS (including multiple scattering effects) for NHdk and FeL(NO)+ gives the following identical results: a single NO bound per iron with r(FeN) = 1.68 +/- 0.03 Angstrom and angle FeNO approximate to 165 degrees. In NHdk, the presence of the NO Ligand lengthens at least one of the Fe-S bonds relative to those in NHlt. These data show that synthetic inorganic complexes can be designed to assume iron coordination geometries very similar to those of the iron center in nitrile hydratase and confirm results from EPR spin-trapping experiments (Odaka, M.; Fujii, K.; Hoshino, M.; Noguchi, T.; Tsujimura, M.; Nagashima, S.; Yohda, M.; Nagamune, T.; Inoue, Y.; Endo, I. J. Am. Chem. Sec. 1997, 119, 3785-3791) that photoactivation of nitrile hydratase includes loss of a single NO ligand from the iron.