Unusual Synthetic Pathway for an {Fe(NO)₂}⁹Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy

Abstract

Dinitrosyl iron complexes (DNICs) are among the most abundant NO-derived cellular species. Monomeric DNICs can exist in the {Fe(NO)2}(9) or {Fe(NO)2}(10) oxidation state (in the Enemark-Feltham notation). However, experimental studies of analogous DNICs in both oxidation states are rare, which prevents a thorough understanding of the differences in the electronic structures of these species. Here, the {Fe(NO)2}(9) DNIC [Fe(dmp)(NO)2](OTf) (1; dmp = 2,9-dimethyl-1,10-phenanthroline) is synthesized from a ferrous precursor via an unusual pathway, involving disproportionation of an {FeNO}(7) complex to yield the {Fe(NO)2}(9) DNIC and a ferric species, which is subsequently reduced by NO gas to generate a ferrous complex that re-enters the reaction cycle. In contrast to most {Fe(NO)2}(9) DNICs with neutral N-donor ligands, 1 exhibits high solution stability and can be characterized structurally and spectroscopically. Reduction of 1 yields the corresponding {Fe(NO)2}(10) DNIC [Fe(dmp)(NO)2] (2). The Mössbauer isomer shift of 2 is 0.08 mm/s smaller than that of 1, which indicates that the iron center is slightly more oxidized in the reduced complex. The nuclear resonance vibrational spectra (NRVS) of 1 and 2 are distinct and provide direct experimental insight into differences in bonding in these complexes. In particular, the symmetric out-of-plane Fe-N-O bending mode is shifted to higher energy by 188 cm(-1) in 2 in comparison to 1. Using quantum chemistry centered normal coordinate analysis (QCC-NCA), this is shown to arise from an increase in Fe-NO bond order and a stiffening of the Fe(NO)2 unit upon reduction of 1 to 2. DFT calculations demonstrate that the changes in bonding arise from an iron-centered reduction which leads to a distinct increase in Fe-NO π-back-bonding in {Fe(NO)2}(10) DNICs in comparison to the corresponding {Fe(NO)2}(9) complexes, in agreement with all experimental findings. Finally, the implications of the electronic structure of DNICs for their reactivity are discussed, especially with respect to N-N bond formation in NO reductases.

Synthesis, X-ray Structures, Electronic Properties, and O2/NO Reactivities of Thiol Dioxygenase Active-Site Models

“…DFT is known to overestimate ν(NO) frequencies, with hybrid functionals generally performing worse than nonhybrid functionals. 94,101 While our results follow this pattern, the BP86 functional proved quite effective in estimating the energy splitting between the in-phase and out-of-phase combinations of ν(NO) modes of RT NO . Both functionals yielded rhombic g -tensors centered near g = 2.03, consistent with our EPR data and prior studies of DNICs.…”

“…Both functionals yielded rhombic g -tensors centered near g = 2.03, consistent with our EPR data and prior studies of DNICs. 91–94 The computed A -tensors are highly anisotropic with two small A -values (< 10 MHz) and one moderate value of 25 or 39 MHz, in accordance with the absence of any detectable 14 N hyperfine splitting in the experimental RT NO EPR spectrum.…”

“…91–94 Like RT NO , these S = 1/2 {Fe(NO) 2 } 9 species commonly exhibit a rhombic g -tensor centered at 2.03 and a broad absorption band in the near-IR region with an extinction coefficient of ~100 M −1 cm −1 . To determine whether RT NO corresponds to a DNIC, IR spectra of NO-treated 1 and 2 were measured at RT.…”

“…Furthermore, the separation between NO stretching frequencies (Δν NO ) is diagnostic of coordination number and nuclearity, 95 and the Δν NO -value of 72 cm −1 measured for RT NO is typical of four-coordinate (4C) {Fe(NO) 2 } 9 species. 91–94 …”

“…94 Geometry optimizations of the high-spin {FeNO} 7 adduct obtained upon NO binding to 2 yielded quasi-6C structures, labeled S =3/2 [ 2-NO ] 6C , with an elongated distance of 2.5 Å for the Fe–N TIP bond trans to the nitrosyl (Table S4) – indicative of the strong trans influence of NO ligands. 96 Interestingly, during the BP86 geometry optimizations of the low-spin {FeNO} 7 adduct, the trans imidazole fully dissociated and formed an intramolecular H-bond with the amine group of CysAm, yielding the 5C structure S =1/2 [ 2-NO ] 5C .…”