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Cite This: Inorg. Chem. 2019, 58, 9586−9591
NO-to-[N2O2]2−-to‑N2O Conversion Triggered by {Fe(NO)2}10-{Fe(NO)2}9 Dinuclear Dinitrosyl Iron Complex Wun-Yan Wu,† Chia-Ning Hsu,† Chieh-Hsin Hsieh,† Tzung-Wen Chiou,*,† Ming-Li Tsai,*,§ Ming-Hsi Chiang,‡ and Wen-Feng Liaw*,† †
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Department of Chemistry and Frontier Research Center of Fundamental and Applied Science of Matters, National Tsing Hua University, Hsinchu 30013, Taiwan § Department of Chemistry, National Sun Yat-sen University, Kaohsiung 80424, Taiwan ‡ Institute of Chemistry, Academia Sinica, Nankang, Taipei 115, Taiwan S Supporting Information *
Dinitrosyl iron complexes (DNICs) stabilized in the form of protein-bound DNICs and low-molecular-weight dinitrosyl iron complexes (LMW-DNICs) existing in cells have been demonstrated as intrinsic NO-storage/NO-transport species in the biological systems.11,12 The recently developed synthetic methodologies uncover the potential of mononuclear DNICs to mediate chemical reactions associated with reversible oneelectron redox processes ({Fe(NO)2}9 ↔ {Fe(NO)2}10 ↔ [{Fe(NO)2}10-L•]−) and to expand the dinuclear DNICs into three accessible redox states ([{Fe(NO) 2 } 9 -{Fe(NO)2}9] ↔ [{Fe(NO)2}9-{Fe(NO)2}10] ↔ [{Fe-(NO)2}10{Fe(NO)2}10]), where the Enemark−Feltham notation is adopted.13,14 Also, we demonstrate that the reversible {Fe(NO)2}9 ↔ {Fe(NO)2}10 redox shuttling of DNIC modulates nitrite binding modes to trigger nitrite activation, generating nitric oxide.15 It is noted that the NO ligands bound to Fe in mononuclear DNICs do not voluntarily form a reductive coupling product (i.e., hyponitrite), because of their spin-parallel electronic structure of two NO-coordinated ligands in the [Fe(NO)2] unit.16 In this manuscript, the electronically localized, singly alkoxide-bridged {Fe(NO)2}10{Fe(NO) 2 } 9 dinuclear DNIC [(NO) 2 Fe(μ-bdmap)Fe(NO)2(THF)] (bdmap = 1,3-bis(dimethylamino)-2-propanolate) serving as an active center to drive nitric oxide reduction, yielding the paramagnetic hyponitrite-coordinated {[(NO)2Fe(μ-bdmap)Fe(NO)2]2(κ4-N2O2)} intermediate and the subsequent protonation producing N2O and [Fe(NO)2(μbdmap)]2 are delineated. Consistent with the formation of [(μ-S(CH2)2NH2)Fe(NO)2]2 via the reaction of [Fe(CO)2(NO)2] and cysteamine,17 the addition of 1 equiv of Hbdmap (1,3-bis(dimethylamino)-2-propanol) into [Fe(CO)2(NO)2] in tetrahydrofuran (THF) at ambient temperature resulted in the generation of the thermally stable {Fe(NO)2}9-{Fe(NO)2}9 dinuclear DNIC [Fe(NO)2(μ-bdmap)]2 (1), characterized by infrared (IR) spectroscopy (νNO 1721 s, 1653 s cm−1 (THF)) and single-crystal X-ray diffraction (see Scheme 1a, as well as Figures S1 and S2 in the Supporting Information), and hydrogen, as identified by gas chromatography. Electron paramagnetic resonance (EPR) silence and diamagnetism of
ABSTRACT: Flavodiiron nitric oxide reductases (FNORs) evolved in some pathogens are known to detoxify NO via two-electron reduction to N2O to mitigate nitrosative stress. In this study, we describe how the electronically localized {Fe(NO)2}10-{Fe(NO)2}9 dinuclear dinitrosyl iron complex (dinuclear DNIC) [(NO)2Fe(μ-bdmap)Fe(NO)2(THF)] (2) (bdmap = 1,3-bis(dimethylamino)-2-propanolate) can induce a reductive coupling of NO to form hyponitrite-coordinated tetranuclear DNIC, which then converts to N2O. Upon the addition of 1 equiv of NO into the dinuclear {Fe(NO)2}10-{Fe(NO)2}9 DNIC 2, the proposed sideon-bound [NO]−-bridged [(NO)2Fe(μ-bdmap)(κ2-NO) Fe(NO)2] intermediate may facilitate intermolecular (O)N−N(O) bond coupling to yield the paramagnetic tetranuclear quadridentate trans-hyponitrite-bound {[(NO)2Fe(μ-bdmap)Fe(NO)2]2(κ4-N2O2)} that transforms to [Fe(NO)2(μ-bdmap)]2, along with the release of N2O upon Hbdmap (1,3-bis(dimethylamino)-2-propanol) added.
N
itric oxide (NO) reduction yielding nitrous oxide (N2O) triggered by nonheme/heme nitric oxide reductases (NORs) and nonheme flavodiiron nitric oxide reductases (FNORs) is recognized as the process of relieving nitrosative stress for pathogenic bacteria and fungi.1 The catalytic pathways, NO coordination to metal, and then (O)N−N(O) bond coupling producing a hyponitrite intermediate, followed by the N−O bond cleavage of hyponitrite, have been proposed in the chemistry of NO reduction conversion to N2O.1−3 Biomimetic model studies of the mechanism of NO reduction yielding N2O for Fe-, Co-, Ni-, Cu-, Ru-, and Pt-containing complexes propose that the formation of hyponitrite [N2O2]2−-bound intermediate via the coupling of a metal− nitrosyl motif with exogenous NO gas or intramolecular/ intermolecular (O)N−N(O) coupling reaction of two reduced metal-NO units may be adopted.4−9 In our recent study, the reactivity of the reduced-form Fe(II)−Fe(II) microbial protein YtfE toward nitric oxide demonstrates that the prerequisite for N2O production requires the cooperative nitrosylation of two Fe sites prior to their reductive coupling to produce N2O.10 © 2019 American Chemical Society
Received: June 3, 2019 Published: July 11, 2019 9586
DOI: 10.1021/acs.inorgchem.9b01635 Inorg. Chem. 2019, 58, 9586−9591
Communication
Inorganic Chemistry Scheme 1
lability of intermediate A/B with the proposed bridged [NO]−bound [{FeIII(NO−)2}9]2 electronic structure was also demonstrated by the conversion of [Fe(15NO)2(μ-bdmap)Fe(15NO)2(THF)] (2-15NO) into the scrambled products 3-14/15NO upon exposing the THF solution of 2-15NO to 14 NO (1:1 molar ratio) at 0 °C (see the Experimental Section and Figure S7 in the Supporting Information). As opposed to the Fe K-edge pre-edge energy of {Fe(NO)2}10-{Fe(NO)2}9 DNIC 2 that is observed at 7113.5 eV, the distinct Fe K-edge pre-edge energy (7113.9 eV) exhibited by complexes 3 and 1 may suggest that the electronic structure of complexes 3 and 1 may be qualitatively described by the {Fe(NO)2}9-{Fe(NO)2}9 electronic configuration (see Figure S8 in the Supporting Information).13,18,19 A broad, isotropic EPR signal at g = 2.025, accompanied by a half-field signal at g = 4.28 (77 K (solid)) (Figure 1), and the corresponding temperature-dependent μeff
the magnetic measurements of complex 1 is in accord with the 1 H NMR spectrum, displaying the expected signals (δ 3.41 (O−CH), 2.47 (−CH2−), 2.21 (N−CH3) and 3.41 (O−CH), 2.47 (br, −CH2−), 2.15−2.24 (N−CH3) ppm) at 298 and 198 K for bdmap ligands, respectively (see Figures S3 and S4 in the Supporting Information). In contrast to the fully delocalized mixed- valence {F e (NO) 2 } 1 0 - { F e ( N O ) 2 } 9 [F e 2 (μStBu)2(NO)4]− displaying an axial EPR signal (g⊥ = 2.009 and g|| = 1.965) at 77 K and IR νNO 1673 s, 1655 s (THF),13c upon the addition of 2 equiv of [Fe(CO)2(NO)2] into complex 1 or the addition of 2 equiv of [Fe(CO)2(NO)2] into Hbdmap in THF (Schemes 1b and 1c), the isotropic EPR spectrum (g = 2.016 (solid) at 77 K) and the IR νNO (cm−1) 1762 m, 1701 s, 1682 sh, 1650 s (THF) suggest the generation of the singly O-bdmap-bridged, electronically localized {Fe(NO)2}10-{Fe(NO)2}9 dinuclear DNIC [Fe(NO)2(μ-bdmap)Fe(NO)2(THF)] (2) with [Fe(NO)2]9 unit coordinated by solvent THF (see Figures S5 and S6 in the Supporting Information). The noninnocent character of NO ligands serving as electron buffer may attenuate the polarization of the five-coordinated THF-bound Fe center induced by the Fe−Oμ‑bdmap bond, such that the highly covalent {Fe(NO)2}9 core of complex 2 is preserved.18,19 Presumably, the poor covalency of the Fe−Oμ‑bdmap bond may play a key role in building/stabilizing the electronically localized {Fe(NO)2}10-{Fe(NO)2}9 dinuclear DNIC 2, which promotes the electrophilic attack of NO on the {Fe(NO)2}10 core (NO reduction).18 As shown in Scheme 1d, the injection of NO gas into the THF solution of complex 2 (1:1 molar ratio) by a gas-tight syringe at 0 °C led to the precipitation of brown microcrystals characterized as a trans-hyponitritebridged {[Fe(NO)2]2(μ-bdmap)}2(κ4-N2O2) (3). Complex 3 was generated, presumably via intermediate [(NO)3Fe(μbdmap)Fe(NO)2] (A) → [(NO)2Fe(μ-bdmap)(κ2-NO) Fe(NO)2] (B) intermediate bearing side-on-bridged nitroxyl [NO]− ligand and accompanied by intermolecular (O)N− N(O) coupling (Scheme 1d). The IR νNO stretching frequencies and pattern (IR 1744 s, 1721 s, 1669 s, 1644 s (νNO), 1087 s (νN−O([N2O22−])) cm−1 (KBr)) of complex 3 support that DNIC 2-mediated NO reduction yields hyponitrite-ligated complex 3 (Figure S7 in the Supporting Information). Buildup of the proposed side-on [NO]−-bridged intermediate B, followed by intermolecular (O)N−N(O) coupling, establishes a facile pathway for NO-to-[N2O2]2− conversion. Attempts made to detect the proposed intermediates A/B by FTIR were unsuccessful. The NO ligand
Figure 1. X-band electron paramagnetic resonance spectra (solid) of {[Fe(NO)2]2(bdmap)}2(κ4-N2O2) (3) at 77 K (giso = 2.025) and a half-field signal (g = 4.28) shown in inset.
value of 3.84 μB displayed by complex 3 may result from the weak magnetic coupling (dipolar coupling) among four {Fe(NO)2}9 (S = 1/2) centers (see Scheme 2, as well as Scheme 2
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Inorganic Chemistry Figures S9 and S10 in the Supporting Information). The J1 and J2 values shown in Scheme 2 are determined as −69.8 ± 4.4 cm−1 and −33.8 ± 2.2 cm−1, respectively, from a theoretical fitting of magnetic susceptibility, as a function of temperature (see the Experimental Section and Figure S10 in the Supporting Information). As shown in Scheme 1e, the THF solution of complex 3 was treated with 2 equiv of Hbdmap at ambient temperature and subjected to IR analysis of the headspace, and the reaction solution demonstrated the formation of N2O gas (IR 2223 cm−1 for νNN, 2154 cm−1 for ν15N15N) (see Figures S11 and S12 in the Supporting Information),4−9 and the diamagnetic complex 1 with 82% yield isolated from the reaction solution, in accordance with protonation of [N2O2]2− inducing N2O release (86% yield, as identified by GC and shown in Figure S13 in the Supporting Information). The thermal ellipsoid plot of complex 3 is depicted in Figure 2, and the selected bond lengths and bond angles are presented
N atoms, respectively, while a N(3)−N(3#) bond length of 1.279(5) Å and a N(3)−O(3) bond distance of 1.330(3) Å feature a dianionic hyponitrite-bridged ligand with N(3)− N(3#) double bond character (see Table S1 in the Supporting Information).4−9 Density functional theory (DFT) calculations were conducted to obtain the detailed electronic structure of complex 3. The initial coordinates of complex 3 for DFT geometry optimization were taken from the experimental single-crystal X-ray diffraction (XRD). The bond distances of coordinated hyponitrite in DFT optimized structure agree excellently with the experimental metric parameters (exp: Fe−NN 2O 2 = 2.143(3) Å, N−ON2O2 = 1.330(3) Å, N−NN2O2 = 1.279(5) Å; calc: Fe−NN2O2 = 2.144 Å, N−ON2O2 = 1.318 Å, N−NN2O2 = 1.271 Å), where bond distances of Fe−NNO and N−ONO are slightly overestimated (exp: average Fe−NNO = 1.706 Å, N− ONO = 1.168 Å; calc: average Fe−NNO = 1.755 Å, N−ONO = 1.178 Å) (see Figure S14a and Table S3 in the Supporting Information). The optimized DFT structure was spectroscopically calibrated with experimental IR spectra (exp: average νNO = 1695 cm−1, νas [N2O2] = 1087 cm−1; calc: average νNO = 1711 cm−1, νas[N2O2] = 1095 cm−1) and reasonably consistent with the experimental results. Based on the spin density distribution of complex 3 (broken symmetry singlet state) (Table S4 in the Supporting Information), the coupling interactions of unpaired electrons are best described as an antiferromagnetic coupling of two bdmap-bridged {Fe(NO)2}9 units and antiferromagnetic coupling of two [{Fe(NO)2}9{Fe(NO)2}9] units bridged via dianionic [N2O2]2−, consistent with the fitting of the experimental magnetic susceptibility measurements (see Scheme 2). In order to interrogate the possible intermediate facilitating the formation of complex 3 via N−N bond-coupling pathway, a relaxed potential energy surface scan (singlet state with broken symmetry wave function) along the N−N bond elongation of the coordinated hyponitrite in complex 3 was conducted. As shown in Figures S14b and S15 in the Supporting Information, the elongation of N−NN2O2 starting from the experimental N−N bond distance significantly increases the potential energy and reaches a plateau at N− NN2O2 ≈ 2.6 Å yielding two corresponding [NO]-bridged [{Fe(NO)2}9]2 species (4) (see Table S3 in the Supporting Information). Note that the ground state of species 4 is best described as singlet state with broken-symmetry wave function. The energy of its triplet state is slightly higher than that of the broken symmetry singlet state (∼5 kcal/mol). To elucidate the electronic structure of [NO]-bridged [{Fe(NO)2}9]2 species 4, the bridged NO is computationally moved away from dinuclear [{Fe(NO)2}]2 fragment in the form of NO radical, resulting in an energy increase of ∼20.5 kcal/mol (Figure 3) and the formation of the corresponding geometry-optimized [{Fe(NO)2}9-{Fe(NO)2}10](•NO) (5) DFT structure (Figure S14c and Table S3 in the Supporting Information). As shown in Figure 3, and displayed in Table 1, analysis of the changes of natural charge and spin density among [{Fe(NO) 2 } 9 -{Fe(NO) 2 } 10 ]( • NO) (5), [NO]-bound [{Fe(NO) 2 } 9 ] 2 (4), and trans-hyponitrite-bridged {[Fe(NO)2]2(μ-bdmap)}2(κ4-N2O2) (3) indicate that the coordination of exogenous NO radical to the electronically localized [{Fe(NO)2}9-{Fe(NO)2}10] (natural charge: Fe1, +0.26; Fe2, −0.01; NNO, 0.17; ONO, −0.17) core induces significant charge
Figure 2. ORTEP drawing and labeling scheme of {[Fe(NO)2]2(bdmap)}2(κ4-N2O2) (3) with the thermal ellipsoid drawn at 50% probability. Hydrogen atoms are omitted for clarity. Selected bond lengths (Å): N(1)−O(1), 1.167(4); N(2)−O(2), 1.164(4); N(4)−O(4), 1.170(4); N(5)−O(5), 1.168(4); Fe(1)−N(1), 1.706(3); Fe(1)−N(2), 1.695(3); Fe(2)−N(4), 1.710(3); Fe(2)− N(5), 1.711(3); Fe(1)···Fe(2), 3.493; Fe(1)···Fe(1#), 5.130; Fe(2)··· Fe(2#), 6.736; Fe(1)−N(3), 2.143(3); Fe(2)−O(3), 2.034(2); N(3)−O(3), 1.330(3); and N(3)−N(3#), 1.279(5). Selected bond angles (deg): N(3)−N(3#)−O(3), 112.8(3); Fe(1)−O(6)−Fe(2), 118.31(11); N(3)−O(3)−Fe(2), 113.57(18); and O(3)−N(3)− Fe(1), 122.01(19).
in figure captions. Consistent with the published averaged N− O bond length ranging from 1.160(6) to 1.186(7) Å and the averaged Fe−N(O) bond length within the range of 1.661(4)−1.695(3) Å observed in the {Fe(NO) 2 } 9 DNICs,12,13 complex 3 shows the N−O(NO) and Fe−N(NO) bond lengths from 1.164(4) Å to 1.170(4) Å (mean value 1.167(4) Å) and from 1.695(3) Å to 1.711(3) Å (mean value 1.705(3) Å), respectively. Compared to the Fe(1)···Fe(2) distance of 3.199 Å observed in the diamagnetic {Fe(NO)2}9{Fe(NO)2}9 complex 1 (Figure S2 in the Supporting Information), the apparently longer Fe(1)···Fe(2) distance of 3.493 Å (Fe(1)···Fe(1#) distance of 5.130 Å) found in [{Fe(NO)2}9-{Fe(NO)2}9]2 complex 3 rationalizes the less extent of Fe(1)···Fe(2) (and Fe(1)···Fe(1#)) dipolar coupling reflecting the paramagnetic property. The trans-[N2O2]2− ligand of complex 3 is symmetrically coordinated to two [Fe(NO)2(μ-bdmap)Fe(NO)2] motifs through two O and two 9588
DOI: 10.1021/acs.inorgchem.9b01635 Inorg. Chem. 2019, 58, 9586−9591
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.9b01635. Details of experimental methods and materials; FTIR, EPR, XAS, and XRD data collection details (PDF) Accession Codes
CCDC 1912354 for 1 and 1912353 for 3 contain the supplementary crystallographic data for this paper. These data can be obtained free of charge via www.ccdc.cam.ac.uk/ data_request/cif, or by contacting The Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge CB2 1EZ, UK; fax: + 44 1223 336033.
Figure 3. Proposed reaction coordinate of trans-N,O-hyponitritebridged complex 3 via a N−N coupling pathway.
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AUTHOR INFORMATION
Corresponding Authors
of the bridged NO of [NO]-bridged [{Fe(NO)2}9]2 species (natural charge: Fe1, +0.23; Fe2, +0.39; NNO, +0.05; ONO, −0.32), suggesting the [NO]−-bridged [{Fe(NO)2}9]2 electronic structure. In addition to the charge transfer from the Fe center to the bridged NO upon coordination of NO radical to [{Fe(NO)2}9-{Fe(NO)2}10] unit, the spin density of bridged NO also drastically increases from 5 to 4 (for 5: Fe1, +2.75; Fe2, −1.76; NNO, −0.72; ONO, −0.28; for 4: Fe1, +2.79; Fe2, +2.98; NNO, −1.01; ONO, −0.40). Noticeably, the NO-bridged binding inducing the spin polarization toward the N end of NO, compared to the free NO radical, may facilitate N−N radical coupling to generate trans-hyponitrite-bridged {[Fe(NO)2]2(μ-bdmap)}2(κ4-N2O2) (3). As a result, the spin density of the coordinated [N2O2]2− in 3 reduces to 0.12 (natural charge of 3: Fe1, +0.50; Fe2, +0.35; NNO, +0.10; ONO, −0.50; spin density of 3: Fe1, −3.15; Fe2, +3.03; NNO, +0.10; ONO, −0.04). In summary, the electronically localized {Fe(NO)2}10{Fe(NO)2}9 dinuclear DNIC 2 built/stabilized by the polarization effect of bdmap-bridged ligand was isolated from the reaction of complex 1 and 2 equiv of [Fe(NO)2(CO)2] in THF. Complex 2 triggering NO reduction to generate the paramagnetic tetranuclear DNIC-bound complex 3 ligated by trans-N,O-hyponitrite via intermolecular (O)N−N(O) coupling of intermediate B is demonstrated to be a potential model for providing insight into the mechanism of NORs and the systematic reactivity study of hyponitrite-bound complexes. Subsequent reaction of complex 3 and 2 equiv of Hbdmap in THF quantitatively transforming to complex 1, along with the release of N2O, completes a synthetic cycle 1 → 2 → 3 → 1 for the conversion of NO to N2O.
*E-mail:
[email protected] (T.-W. Chiou). *E-mail:
[email protected] (M.-L. Tsai). *E-mail: fl
[email protected] (W.-F. Liaw). ORCID
Tzung-Wen Chiou: 0000-0001-9764-1127 Ming-Li Tsai: 0000-0003-2510-2866 Ming-Hsi Chiang: 0000-0002-7632-9369 Wen-Feng Liaw: 0000-0001-9949-8344 Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We gratefully acknowledge financial support from Ministry of Science and Technology, and the Featured Area Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) (Taiwan). We also thank the National Synchrotron Radiation Research Center (Taiwan) and the National Center for High-Performance Computing for their support on the hardware and software applied in this work. The authors thank Mr. TingShen Kuo (NTNU) for single-crystal X-ray structural determinations and Dr. Fu-Te Tsai (NTHU) for help in XAS.
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REFERENCES
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Table 1. Selected Spin Density and Natural Charge of Optimized Complexes 3, 4, and 5, Corresponding to Figure 3 [{Fe(NO)2}9-{Fe(NO)2}10](•NO) (5)
[NO]−-Bound [{Fe(NO)2}9]2(4)
{Fe(NO)2]2(-bdmap)}2(κ4-N2O2) (3)
Fe1
Fe2
NO
Fe1
Fe2
NO
Fe1
Fe2
NO
spin density
2.75
−1.76
−0.72(N) −0.28 (O)
2.79
2.98
−0.75 (N) −0.60 (O)
−3.15
3.03
0.10 (N) −0.04
natural
0.26
−0.01
0.17 (N)
0.23
0.39
0.05 (N)
0.50
0.35
0.10 (N)
charge
−0.17 (O)
−0.32 9589
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DOI: 10.1021/acs.inorgchem.9b01635 Inorg. Chem. 2019, 58, 9586−9591
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Inorganic Chemistry Complex (DNIC) and Thiol: Facile Synthetic Route for Synthesizing Cysteine-Containing DNIC. Inorg. Chem. 2013, 52, 13918−13926. (18) Liu, P.-H.; Tsai, F.-T.; Chen, B.-H.; Hsu, I.-J.; Hsieh, H.-H.; Liaw, W.-F. Insight into Chalcogenolate-Bound {Fe(NO)2}9 Dinitrosyl Iron Complexes (DNICs): Covalent Character versus Ionic Character. Dalton Trans 2019, 48, 6040−6050. (19) Tsai, M.-C.; Tsai, F.-T.; Lu, T.-T.; Tsai, M.-L.; Wei, Y.-C.; Hsu, I.-J.; Lee, J.-F.; Liaw, W.-F. Relative Binding Affinity of Thiolate, Imidazolate, Phenoxide, and Nitrite Toward the{Fe(NO)2} Motif of Dinitrosyl Iron Complexes (DNICs): The Characteristic Pre-Edge Energy of {Fe(NO)2}9 DNICs. Inorg. Chem. 2009, 48, 9579−9591.
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DOI: 10.1021/acs.inorgchem.9b01635 Inorg. Chem. 2019, 58, 9586−9591
