Spectroscopic Studies of the Effect of Ligand Donor Strength on the Fe−NO Bond in Intradiol Dioxygenases

• Published in: Inorganic chemistry 2003-01, Vol.42 (2), p.365-376
• Main Authors: Wasinger, Erik C, Davis, Mindy I, Pau, Monita Y. M, Orville, Allen M, Zaleski, Jeffrey M, Hedman, Britt, Lipscomb, John D, Hodgson, Keith O, Solomon, Edward I
• Format: Article
• Language: English
• Subjects: Algorithms; Binding Sites; Circular Dichroism; Crystallography, X-Ray; Iron - chemistry; Ligands; Models, Molecular; Molecular Conformation; Oxidation-Reduction; Protocatechuate-3,4-Dioxygenase - chemistry; Spectroscopy, Fourier Transform Infrared; Spectrum Analysis
• ISSN: 0020-1669; 1520-510X
• DOI: 10.1021/ic025906f

The geometric and electronic structure of NO bound to reduced protocatechuate 3,4-dioxygenase and its substrate (3,4-dihydroxybenzoate, PCA) complex have been examined by X-ray absorption (XAS), UV−vis absorption (Abs), magnetic circular dichroism (MCD), and variable temperature variable field (VTVH) MCD spectroscopies. The results are compared to those previously published on model complexes described as {FeNO}7 systems in which an S = 5/2 ferric center is antiferromagnetically coupled to an S = 1 NO-. XAS pre-edge analysis indicates that the Fe−NO units in FeIIIPCD{NO-} and FeIIIPCD{PCA,NO-} lack the greatly increased pre-edge intensity representative of most {FeNO}7 model sites. Furthermore, from extended X-ray absorption fine structure (EXAFS) analysis, the FeIIIPCD{NO-} and FeIIIPCD{PCA,NO-} active sites are shown to have an Fe−NO distance of at least 1.91 Å, ≈0.2 Å greater than those found in the model complexes. The weakened Fe−NO bond is consistent with the overall lengthening of the bond lengths and the fact that VTVH MCD data show that NO- → FeIII CT transitions are no longer polarized along the z-axis of the zero-field splitting tensor. The weaker Fe−NO bond derives from the strong donor interaction of the endogenous phenolate and substrate catecholate ligands, which is observed from the increased intensity in the CT region relative to that of {FeNO}7 model complexes, and from the shift in XAS edge position to lower energy. As NO is an analogue of O2, the effect of endogenous ligand donor strength on the Fe−NO bond has important implications with respect to O2 activation by non-heme iron enzymes.