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Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX
Stable Ferrous Mononitroxyl {FeNO}8 Complex with a Hindered Hydrotris(pyrazolyl)borate Coligand: Structure, Spectroscopic Characterization, and Reactivity Toward NO and O2 Kiyoshi Fujisawa,*,† Shoko Soma,†,∥ Haruka Kurihara,† Ayuri Ohta,† Hai T. Dong,‡,∥ Yurika Minakawa,† Jiyong Zhao,§ E. Ercan Alp,§ Michael Y. Hu,§ and Nicolai Lehnert*,‡ †
Department of Chemistry, Ibaraki University, Mito 310-8512, Japan Department of Chemistry and Department of Biophysics, University of Michigan, Ann Arbor, Michigan 48109, United States § Advanced Photon Source, Argonne National Laboratory, Argonne, Illinois 60439, United States
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‡
S Supporting Information *
Herein, we report a novel four-coordinate (4C) hs-{FeNO}8 complex, [Fe(NO)(L3)] (1), which is surprisingly stable and constitutes the first and only example of its kind that could be structurally characterized.7 This complex shows interesting reactivities, as described in this paper, particularly a very unusual equilibrium with a dinitrosyl iron compound (DNIC). Complex 1 uses the highly hindered hydrotris(pyrazolyl)borate coligand, hydrotris(3-tertiary butyl-5-isopropyl-1-pyrazolyl)borate anion (L3− in Figure S1), which enables 4C structures because of the second coordination sphere protection by bulky tertiary butyl groups.8 By using this ligand, we previously reported 4C hs transition-metal nitrosyl complexes [M(NO)(L3)] with M = Co, Ni, and Cu, with detailed spectroscopic and computational analyses (see Figure S2 and Tables S1 and S2). Starting from a ferrous precursor complex with the highly hindered L3− ligand, we cannot synthesize any nitrosyl complex by the simple reaction with NO gas. Instead, complex 1 was obtained by reaction of [Fe(NO)2(μ-I)]29 with the potassium salt of the ligand L3− (Scheme 1). A number of lowspin (ls) non-heme {FeNO}8 complexes have been prepared;6 however, as mentioned before, hs-{FeNO}8 complexes are rare,7 and none of them are stable enough for structural characterization. These complexes typically undergo direct N− N coupling or disproportionation into DNICs.7 The enhanced
ABSTRACT: The iron(II)-nitroxyl complex [Fe(NO)(L3)] (1) (with L3− = a hindered hydrotris(pyrazolyl)borate ligand), a high-spin (hs)-{FeNO}8 complex in the Enemark−Feltham notation, is surprisingly stable and is the first of its kind that could be structurally characterized. We further studied this compound using a variety of spectroscopic methods. These results indicate a hs iron(II) center with a bound 3NO− ligand where the spins are antiferromagnetic coupled (St = 1). Vibrational data show that this complex has a very strong Fe−NO bond. DFT calculations support this result and link it to very strong π-donation from the 3NO− ligand to the iron(II) center. Furthermore, a very unusual equilibrium between the hs-{FeNO}8 complex and a dinitrosyl iron complex (DNIC) of {Fe(NO)2}9 type is observed. The O2 reactivity of the complex is finally reported.
N
itric oxide (NO) plays pivotal roles in a variety of physiological processes related to signaling and immune defense.1 Moreover, •NO has one unpaired electron, so this diatomic can react with transition-metal ions to form a range of coordination complexes,2 which can exist in the form of different valence tautomers. To overcome this ambiguity, the Enemark-Feltham notation, {M(NO)x}n, was developed (with x = number of nitrosyl ligand(s) and n = metal-d plus nitrosylπ* electrons) and is now widely used.3 In biology, Fe−NO interactions occur in a multitude of proteins such as flavodiiron proteins (FDPs), nitric oxide reductases, NO transporters, nitrite reductases, NO sensors and NO-responsive transcription factors.4 Many Fe−NO model complexes in the {FeNO}7 redox state with a variety of non-heme ligands have been synthesized and characterized in detail.2,5−7 Compared to this plethora of non-heme high-spin (hs) {FeNO}7 complexes, not much is known about these complexes in other oxidation states. However, recent work on FDPs and a corresponding, functional model complex implicate the presence of hs{FeNO}8 complexes in NO reductase chemistry.2 So far, only two corresponding non-heme hs-{FeNO}8 compounds have been reported, which are unstable, reactive species in solution, with a proposed St = 1 ground state.7 © XXXX American Chemical Society
Scheme 1
Received: January 12, 2019
A
DOI: 10.1021/acs.inorgchem.9b00107 Inorg. Chem. XXXX, XXX, XXX−XXX
Communication
Inorganic Chemistry
of the characteristic d-d transitions for hs-Fe(II) in the NIR region strongly indicates the oxidation state of Fe in 1 is +II. To further confirm the assignment of the St = 1 ground state for complex 1, the 1H NMR spectra of both [Fe(Cl)(L3)] and 1 were collected (Figures S12 and 13). The paramagnetic 1H NMR spectra of [Fe(Cl)(L3)] show resonances in the range from 66.0 ppm to −8.6 ppm (Figure S12).10 In contrast, relatively sharp signals and smaller paramagnetic shifts are observed in the 1H NMR spectra of 1, from 31.6 to −12.3 ppm (Figure S13), showing a lower spin state compared to [Fe(Cl)(L3)] (St = 2). The total spin of the complex should be St = 1, originating from antiferromagnetic (AF) coupling between the d-electrons of hs-Fe(II) and the π*-electrons of the reduced nitroxyl ligand (3NO−), which has a spin of S = 1.8 Using the Evans method, a magnetic moment of 3.13 μB is determined, supporting an St = 1 ground state for 1. To obtain more insight into the electronic structure of 1, density functional theory (DFT) calculations were performed using different methods. As shown in Table S3, BP86 gives the closest agreement with the structural parameters of the Fe− N−O unit in the crystal structure, especially the Fe−NO (expt 1.675 versus 1.667 Å calcd) and N−O bond lengths (exp. 1.187 vs 1.193 Å calculated). BP86 also reproduces the N−O stretching frequency well (exp. 1696 cm−1 versus 1712 cm−1 calcd), whereas the Fe−NO stretching frequency is overestimated (exp. 554 cm−1 versus 607 cm−1 calculated), which is not unusual with this functional.12 In order to contrast the electronic structure of 1 with our reference compound 2, we then performed B3LYP/TZVP single points on the BP86optimized structures of both compounds. Figure 2 shows the resulting MO diagram for [Fe(NO)(L3)]. This complex exhibits the typical Fe(II)−NO− electronic structure of hs-
stability of 1 is very surprising, thus prompted us to investigate this complex in detail. From X-ray crystallography, the coordination geometry of 1 is distorted tetrahedral with an averaged Fe-Npz bond length of 2.068(1) Å; see Figure 1. This is similar to the 4C chlorido
Figure 1. Crystal structure of [Fe(NO)(L3)] (1) with 50% thermal ellipsoids. Hydrogen atoms are omitted for clarity.
iron(II) complex [Fe(Cl)(L3)] (Figure S3). This is a first indication that the iron center in 1 is in the + II oxidation state. The N41−O41 and Fe1−N41 bond lengths are 1.1865(17) and 1.6753(13) Å, respectively, and the Fe1−N41−O41 unit is essentially linear with an angle of 176.76(18)°. These structural parameters in 1 are different from the only other, structurally characterized (from EXAFS) hs-{FeNO}8 complex [Fe(TMG3tren)(NO)]+ (2; TMG3tren = 1,1,1-tris{2-[N2(1,1,3,3-tetramethylguanidino)]ethyl}amine), which shows an Fe−NO distance of 1.76 Å and a Fe−N−O bond angle of ∼150°.7b The linear Fe−N−O unit in 1 may relate to the lack of a trans ligand compared to 2.7b The ν(N−O) stretch of [Fe(14NO)(L3)] is observed at 1696 cm−1, which shifts (Δ) to 1662 cm−1 (Δν = 34 cm−1) in [Fe(15NO)(L3)] (Figures S4 and S5). The Fe−NO stretching vibration, ν(Fe-NO), is identified at 554 cm−1 in the Far-IR spectra (Figure S6; 550 cm−1 via NRVS; Figure S7) and shifts by 9 cm−1 to lower energy with 15NO. Compared to the other, well characterized hs-{FeNO}8 complex 2, complex 1 shows distinctively higher N−O and Fe−NO stretching frequencies (1696 versus 1618 cm−1 and 554 versus 435 cm −1 , respectively), which indicates a stronger, unusually covalent Fe−N−O unit in 1. This is in excellent agreement with the linear Fe−N−O unit in 1, and the unusual stability of this species. UV−vis spectra (in CH2Cl2) and diffuse reflectance (DR) spectra (solid state) of 1 are shown in Figures S8 and S9. The similarities of the UV−vis and DR spectra of 1 indicate that this complex retains its structure in solution compared to the crystal structure. This {FeNO}8 complex exhibits strong absorption bands in the 450 to 700 nm range (Figure S8). Distorted tetrahedral iron(II) model complexes exhibit two ligand-field transitions in the 1430−2500 nm region.10,11 Complex 1 shows corresponding features at 1508 and 1994 nm (∼6600 and 5000 cm−1, respectively). To confirm these assignments, we also measured UV−vis and DR spectra of [Fe(Cl)(L3)] (Figures S10 and S11). This complex shows strong absorption bands at 1522 and 1982 nm. The presence
Figure 2. MO diagram (UCOs) of [Fe(NO)(L3)] (1), showing antiferromagnetic coupling between the hs-Fe(II) center and the 3 NO− ligand. B
DOI: 10.1021/acs.inorgchem.9b00107 Inorg. Chem. XXXX, XXX, XXX−XXX
Communication
Inorganic Chemistry {FeNO}8 complexes, where the iron center is in the hs-Fe(II) state (S = 2), bound to a triplet 3NO− (S = 1), and the spins are antiferromagnetically coupled, resulting in St = 1. In agreement with this assignment, the calculated spin densities are +3.16 on Fe and −1.24 on NO (Table S4). This electronic structure is also reflected in the MO diagram shown in Figure 2. In the hs-Fe(II)−NO− ground state of 1, all α-d orbitals are singly occupied, whereas the NO−(π*) electrons occupy the corresponding β−π* orbitals. The NO− ligand then acts as a strong π-donor, creating a very covalent Fe−NO bond. Correspondingly, the β−π* orbitals have large contributions from the Fe dπ orbitals (about 30%) as shown in Figure 2. This strongly covalent Fe−NO bond is reflected experimentally in the very high Fe−NO stretching frequency of 554 cm−1 in [Fe(NO)(L3)]. In comparison, 2 has a similar electronic structure, but the Fe contribution to the β−π* orbitals of NO− is reduced to ∼24% in the calculations (Table S5), which corresponds to a less-covalent Fe−NO bond. This trend is consistent across multiple functionals. Considering that the Fe−NO stretch of 1 is >100 cm−1 higher in energy than that of 2 (at 435 cm−1), this reduction in the covalency of the Fe−NO bond in 2 is clearly underestimated in the calculations compared to experiment. The highly covalent Fe−NO bond in 1 explains the surprising stability of this compound, which can be crystallized, whereas 2 is unstable and decomposes at room temperature.7b Similar to hs-{FeNO}7 complexes, the donicity of the coligand influences the properties of the Fe−NO unit in hs-{FeNO}8 compounds.12 Since L3− is a much weaker donor than TMG3tren, this causes much stronger π-donation from the 3NO− ligand to Fe(II) in 1 compared to 2. This increase in π-donation is also reflected by the linear Fe−N−O angle in 1. Complex 1 reacts with NO gas in the solution state: after 12 h reaction time, the solution changed color from green to brown, indicating that a new complex has formed. However, upon drying the solution on the vacuum line, the color of the obtained powder turned back to green, and 1 was recovered. The reaction is therefore completely reversible. Solution IR spectroscopy (in CH2Cl2) after the reaction with NO gas showed two N−O stretching vibrations at 1805 and 1732 cm−1, indicating formation of the 5C (or 4C) DNIC [Fe(NO)2(L3)] (Figure S14). Hence, the formation of the unusual hs-{FeNO}8 complex 1 is promoted by the bulky L3− ligand, which renders the corresponding dinitrosyl complex unstable, according to the unusual equilibrium:
obtained with a normal, bidentate binding mode of nitrite (Figure S17). However, the formation of [Fe(κ2-O2NO)(L3)] was also observed, albeit in smaller amounts (Figure S18). If the reaction with O2 is conducted in the solid state, [Fe(κ2O2NO)(L3)] is now the main product (∼76% yield after 24 h) and a small amount of [Fe(κ2-O2N)(L3)] is also formed (Figures S19 and S20). The conversion of NO to NO2− and NO3− is not typical for iron-nitrosyl complexes. We propose that these reactions proceed in analogy to [Co(NO)(L3)] (see Figure S21; via peroxynitrite as the key intermediate).13,14 This reactivity is somewhat similar to that of the analogous Co(II) and Ni(II) nitrosyl complexes [Co(NO)(L3)] and [Ni(NO)(L3)] that we have previously studied.13,15 However, [Fe(NO)(L3)] shows the fastest O2 reactivity in this series of three [M(NO)(L3)] complexes. In summary, we have prepared the new non-heme hs{FeNO}8 complex [Fe(NO)(L3)] that can be, for the first time, structurally characterized. Spectroscopic data and DFT calculations indicate that this complex is best described as hsFe(II)−3NO−. This complex is surprisingly stable compared to the 5C analogue 2 with the TMG3tren coligand, which is explained by the less donating ligand environment, thus leading to a much more enhanced π-donation of the NO− ligand to the hs-Fe(II) center in 1. This is further supported by the spectroscopic and structural data of 1, which has a very short Fe−NO bond with a very high Fe−NO stretching frequency. The unusual reactivity of this complex toward NO and O2 is further reported.
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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.9b00107. Table of additional (reported) metal-nitrosyl complexes, experimental details, and further characterization data of the complexes (crystal structure details, IR, far-IR, NRVS, UV−vis, DR, 1H NMR, spectral changes during the reactions), proposed oxygen atom(s) transfer reaction mechanism, and computational details (PDF) Accession Codes
CCDC 1866552−1866554 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 emailing
[email protected], or by contacting The Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge CB2 1EZ, UK; fax: +44 1223 336033.
[Fe(NO)(L3)] + NO ⥃ [Fe(NO)2 (L3)]
Indeed, with the less hindered dmp (= 2,9-dimethyl-1,10phenanthroline) ligand, dinitrosyl iron complexes are again obtained.5c This result is significant (and unprecedented), as it points toward a new way how non-heme {FeNO}8 species could be formed in biologyby NO release from DNIC precursors.12 Finally, we investigated the reactivity of our model complex 1 with O2. The possibility of transition metal nitrosyl complexes to activate O2 is relevant in the light of the formation of reactive oxygen species.2 After exposing 1 to O2 for 10 min, the color of the solution changed from green to yellow, and the ν(N−O) band of 1 disappeared (Figures S15 and S16). 15NO labeling experiments further confirmed the formation of [Fe(κ2-O2N)(L3)] (79% yield), in agreement with our [Co(NO)(L3)] results.13 From the reaction mixture, single crystals of the product [Fe(κ2-O2N)(L3)] were
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AUTHOR INFORMATION
Corresponding Authors
*E-mail:
[email protected]. *E-mail:
[email protected]. ORCID
Kiyoshi Fujisawa: 0000-0002-4023-0025 Hai T. Dong: 0000-0002-8914-3045 Nicolai Lehnert: 0000-0002-5221-5498 Author Contributions ∥
S.S. and H.T.D. are co-first authors.
Notes
The authors declare no competing financial interest. C
DOI: 10.1021/acs.inorgchem.9b00107 Inorg. Chem. XXXX, XXX, XXX−XXX
Communication
Inorganic Chemistry
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(9) Dahl, L. F.; de Gil, E. R.; Feltham, R. D. Solid-state structures of dinitrosyliron iodide and dinitrosylcobalt iodide: stereochemical consequences of strong metal-metal interactions in ligand-bridged complexes. J. Am. Chem. Soc. 1969, 91, 1653−1664. (10) (a) Matsunaga, Y.; Fujisawa, K.; Ibi, N.; Miyashita, Y.; Okamoto, K. Structural and spectroscopic characterization of first-row transition metal(II) substituted blue copper model complexes with hydrotris(pyrazolyl)borate. Inorg. Chem. 2005, 44, 325−335. (b) Gorelsky, S. I.; Basumallick, L.; Vura-Weis, J.; Sarangi, R.; Hodgson, K. O.; Hedman, B.; Fujisawa, K.; Solomon, E. I. Spectroscopic and DFT investigation of [M{HB(3,5-iPr2pz)3}(SC6F5)] (M = Mn, Fe, Co, Ni, Cu, and Zn) model complexes: Periodic trends in metal−thiolate bonding. Inorg. Chem. 2005, 44, 4947−4960. (11) Pavel, E. G.; Kitajima, N.; Solomon, E. I. Magnetic circular dichroism spectroscopic studies of mononuclear non-heme ferrous model complexes. Correlation of excited- and ground-state electronic structure with geometry. J. Am. Chem. Soc. 1998, 120, 3949−3962. (12) Berto, T. C.; Hoffman, M. B.; Murata, Y.; Landenberger, K. B.; Alp, E. E.; Zhao, J.; Lehnert, N. Structural and electronic characterization of non-heme Fe(II)−nitrosyls as biomimetic models of the FeB center of bacterial nitric oxide reductase. J. Am. Chem. Soc. 2011, 133, 16714−16717. (13) Fujisawa, K.; Soma, S.; Kurihara, H.; Dong, H. T.; Bilodeau, M.; Lehnert, N. A cobalt−nitrosyl complex with a hindered hydrotris(pyrazolyl)borate coligand: detailed electronic structure, and reactivity towards dioxygen. Dalton Trans. 2017, 46, 13273− 13289. (14) Thyagarajan, S.; Incarvito, C. D.; Rheingold, A. L.; Theopold, K. H. In pursuit of a stable peroxynitrite complex−NOx (x = 1−3) derivatives of Tpt‑Bu,MeCo. Inorg. Chim. Acta 2003, 345, 333−339. (15) Soma, S.; Stappen, C. V.; Kiss, M.; Szilagyi, R. K.; Lehnert, N.; Fujisawa, K. Distorted tetrahedral nickel-nitrosyl complexes: spectroscopic characterization and electronic structure. J. Biol. Inorg. Chem. 2016, 21, 757−775.
ACKNOWLEDGMENTS K.F. is grateful for the financial supports from the Japan Society for the Promotion of Science (JSPS) (25109505). N. L. acknowledges support for this work from the National Science Foundation (CHE-1608331).
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DEDICATION Dedicated to Professor Kenneth D. Karlin on the occasion of his 70th birthday.
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REFERENCES
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DOI: 10.1021/acs.inorgchem.9b00107 Inorg. Chem. XXXX, XXX, XXX−XXX
