A Copper(II) Nitrite That Exhibits Change of Nitrite Binding Mode

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Article Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX

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A Copper(II) Nitrite That Exhibits Change of Nitrite Binding Mode and Formation of Copper(II) Nitrosyl Prior to Nitric Oxide Evolution Ram Chandra Maji,† Saikat Mishra,† Anirban Bhandari,† Ravindra Singh,‡ Marilyn M. Olmstead,§ and Apurba K. Patra*,† †

Department of Chemistry, National Institute of Technology Durgapur, Mahatma Gandhi Avenue, Durgapur 713 209, India Department of Chemistry, Indian Institute of Technology (IIT) Kanpur, Kanpur 208 016, India § Department of Chemistry, University of California, Davis, California 95616, United States ‡

S Supporting Information *

ABSTRACT: The proton-coupled reduction of CuII-bound nitrite (NO2−) to nitric oxide (NO2− + 2H+ + e− → NO(g) + H2O), such as occurs in the enzyme copper nitrite reductase, is investigated in this work. Our studies focus on the copper(II/I) model complexes [(L2)Cu(H2O)Cl] (1), [(L2)Cu(ONO)] (2), [(L2)Cu(CH3CO2)] (3), and [Co(Cp)2][(L2)Cu(NO2)(CH3CN] (4), where HL2 = N[2-(methylthio)ethyl]-2′-pyridinecarboxamide. Complex 1 readily reacts with a NO2− anion to form the nitrito-O-bound copper(II) complex 2. Electrochemical reduction of CuII → CuI indicates coordination isomerization from asymmetric nitrito-κ2-O,O to nitroκ1-N. Isolation and spectroscopic characterization of 4 support this notion of nitrite coordination isomerization (νCu−N ∼ 460 cm−1). A reduction of 2, followed by reaction with acetic acid, causes evolution of stoichiometric NO via the transient copper(II) nitrosyl species and subsequent formation of the acetate-bound complex 3. The probable copper nitrosyl intermediate [(L2)Cu(NO)(CH3CN)]+ of the {CuNO}10 type is evident from lowtemperature UV−vis absorption (λmax = 722 nm) and electron paramagnetic resonance spectroscopy. A density functional theory (DFT)-optimized model of [(L2)Cu(NO)(CH3CN)]+ shows end-on NO binding to Cu with Cu−N(NO) and N−O distances of 1.989 and 1.140 Å, respectively, and a Cu−N−O angle of 119.25°, consistent with the formulation of CuII-NO•. A spin-state change that triggers NO release is observed. Considering singlet- and triplet-state electronic configurations of this model, DFTcalculated νNO values of 1802 and 1904 cm−1, respectively, are obtained. We present here important mechanistic aspects of the copper-mediated nitrite reduction pathway with the use of model complexes employing the ligand HL2 and an analogous phenylbased ligand, N-[2-(methylthio)phenyl]-2′-pyridinecarboxamide (HL1).

1. INTRODUCTION

bonded copper(I/II) nitrite structure for the case of enzyme is evident. This route requires only 1 equiv of proton to release NO without forming the {CuNO} intermediate and produces a copper(II) hydroxide product instead of the water-bonded CuII resting state, leaving the catalytic cycle incomplete, unlike route I. Recently, Bernholc et al. shed light on the feasibility of the two routes and proposed that the single N-coordinated copper(I) nitrite is 8.15 kcal mol−1 less in energy than its Ocoordinated copper(I) nitrite form; therefore, the redoxcoupled switching of the nitrite binding mode such as (nitrito-κ2-O,O)CuII → (nitro-κ1-N)CuI is energetically highly favorable, suggesting route I as the most possible pathway for CuNiR function.4 Furthermore, using serial femtosecond crystallography, Fukuda et al. have shown a NO evolution mechanism of CuNiR via both side-on- and end-on-bound {CuNO} species, where the substrate-bound reduced enzyme

1

Copper nitrite reductases (CuNiRs) catalyze the protoncoupled one-electron reduction of nitrite (NO2−) to nitric oxide (NO) and thereby participate in the denitrification process, a key step in the global dinitrogen cycle.2 X-ray structures of CuNiRs3 revealed the presence of two Cu sites, type I (T1) and type II (T2) ca. 12.5 Å away. The T2 site binds NO2− by replacing the water molecule. During catalytic turnover, the T1 site transfers an electron to the T2 site, either prior to or later than the NO2− binding step (paths I and II, Figure 1), thus forming a CuI-NO2 intermediate. This intermediate then reacts with the protons of protein side chains and evolves NO either via the highly unstable copper nitrosyl species of the {CuNO}10 type, route I (orange arrows, Figure 1),3c,g,4,5 or via the protonated copper(I) nitrite species6,7 {CuIHNO2}, route II (purple arrows, Figure 1). The latter route is based on the results of steady-state kinetics and pulsed radiolysis experiments6 and computational study,7 and this route is reasonably invoked to account for the fact that no N© XXXX American Chemical Society

Received: November 13, 2017

A

DOI: 10.1021/acs.inorgchem.7b02897 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

known to date of a structurally characterized {CuNO}10 complex,13 [Cu(CH3NO2)5(NO)](PF6)2, also demonstrates bent, end-on N ligation of NO to CuII. Therefore, evidence of switching the NO2− coordination from κ2-O,O or κ1-O → κ1-N and subsequent NO evolution via a {CuNO}10 species (as suggested for the CuNiR catalytic cycle4,5) with a model complex is remarkable. No nitrito-O-bound copper(I) structure with a biologically relevant N-donor ligand is known that generates NO upon reaction with protons, although a model with a P-donor ligand is reported.14 This latter model features symmetric κ2-O,Obound NO2− unlike that observed in oxidized CuNiR, where asymmetric κ2-O,O binding is found. The former copper(I) model, including the proposed reduced enzymes with nitrito-O coordination (suggested by Suzuki and Hasnain),3d,g is known to produce NO in the presence of protons. The question of whether a change of NO2− ligation, κ2-O,O → κ1-N, occurs in the presence of protons just before the NO2− → NO conversion has remained elusive. No spectroscopic evidence in favor of a NO2− coordination change has been reported, although an analogous mechanism was proposed by Murphy et al.10 for the CuNiR catalytic cycle that was recently predicted by Bernholc et al.4 and others.5 It assumes that Cu-bonded nitrito-O protonation is feasible and that Cu−Onitrite bond breaking, κ2-O,O → κ1-N conversion, and subsequent NO evolution occur via {CuNO} species. In fact, for a model complex with a κ1-N-bound NO2−, a two-step O protonation followed by NO generation is known,9e strongly supporting the proposed O protonation, but at the same time, it raised an important unanswered question (is κ2-O,O → κ1-N conversion of NO2− coordination mandatory for NO generation by CuNiR?), which was recently addressed.4,5 In fact, a recent report proposed no formation of a {CuNO} intermediate, while NO generation occurs from the reaction of a CuI complex (ligated to a tripodal N4-donor ligand) with Ph3SiNO2; NO2− → NO conversion succeeds through the electron/proton transfer taking place in the secondary coordination sphere, strongly supporting the route II mechanism.15 The changes of NO2− binding and subsequent NO generation were reported by us in a preceding paper,16 but any spectroscopic evidence of {CuNO} formation prior to NO evolution with any model complex/enzyme is still absent. To verify the switching of NO2− binding and to gain more insight into the mechanism of NO2− reduction to NO and whether it occurs via a {CuNO} intermediate, we report here the syntheses and structural, spectral, and electrochemical properties including density functional theory (DFT) calculation of copper(II/I) nitrite/nitrosyl complexes supported by a ligand HL2, analogous to HL1 (Scheme 1). The progressive reaction sequence investigated and reported in this paper is shown in Scheme 1, which strongly supports the route I mechanism (Figure 1) for the first time.

Figure 1. Proposed mechanistic pathways for nitrite (κ1-N-, κ2-O,O-, and κ 3 -O,N,O-bound copper(I) nitrite are shown as A−C, respectively) reduction activity of CuNiR (E = enzyme; orange arrows, route I; purple arrows, route II).

has a κ3-O,N,O-bound nitrite, strongly supporting the route I mechanism.5 Several copper(II/I) nitrite model complexes of CuNiR are known.8,9 Various spectroscopic studies, X-ray structure determinations, and theoretical calculations carried out on both the CuNiR enzymes and model complexes have revealed many important aspects of the nitrite reduction pathway, such as the binding mode of nitrite to CuII/I, the necessity of CuII → CuI reduction, the role of conformational changes in the Asp98 protein chain,4 the preference of proton- and electron-transfer processes7 during catalytic turnover, and the sources of electrons and protons responsible for NO evolution. Although such crucial aspects of the overall catalytic pathway are well established, there is a paucity of information on some of the mechanistic aspects of route I, such as the change of the NO2− coordination mode, formation of the transient {CuNO} species prior to NO generation, and NO binding type to CuI/II.4,5 The similarity of the Cu−N(NO2) and Cu−O(NO2) distances3c,e,g has suggested side-on NO coordination to copper, and later the X-ray structure of an NO-bound reduced enzyme10 revealed an unusual side-on NO ligation to CuI, generating a {CuNO}11 species, but the NO binding mode to CuII, generating a {CuNO}10 species, is not structurally evident yet for CuNiR. The pioneering work of Lehnert et al., complemented by the work of Usov et al., has resolved the issue of side-on versus endon NO binding to CuI.11 Potential-energy-surface scanning revealed that the side-on CuI-NO structure lies on a local minimum (which is structurally characterized by Murphy et al.; later it is speculated as a crystal artifact11b,c). However, the endon CuI-NO structure exists on a global minimum;11a thereby the latter structure is energetically more favorable (8.4 kcal mol−1 less in energy than the side-on NO structure) than the former and exists in solution. Similar to {CuNO}11 species, the recent theoretical calculations on enzymes4 and model complexes12 strongly support an end-on N coordination of NO to CuII, producing a {CuNO}10 intermediate. This latest information on end-on NO coordination is vital because in the catalytic cycle a {CuNO}10 species (formulated as CuII-NO• or CuI-NO+) is believed to form, which can produce NO but not the {CuNO}11 species11b (formulated as CuI-NO• or CuII-NO−). The only example

2. EXPERIMENTAL AND COMPUTATIONAL METHODS 2.1. Materials and Reagents. Pyridine-2-carboxylic acid, 2(methylthio)ethylamine, triphenylphosphite, sodium hydride, sodium perchlorate, (n-Bu4N)NO2, and (n-Bu4N)ClO4 were purchased from Aldrich Chemical Co. and used without further purification. CH3CN, CH3OH, CHCl3, C5H5N (pyridine), and (C2H5)2O (diethyl ether) used either for spectroscopic studies or for syntheses were purified and dried following standard procedures prior to use. Tetraphenylporphyrin (TPP) was synthesized following a reported procedure.17 2.2. Syntheses of Ligands and Complexes. 2.2.1. N-[2(Methylthio)ethyl]-2′-pyridinecarboxamide (HL2). To a stirred B

DOI: 10.1021/acs.inorgchem.7b02897 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry Scheme 1. Proposed Mechanistic Pathway for NO2− Reduction to NO by the Model Complexes, Chemdraw Drawing of HL1 and HL2 (H Is a Dissociable Amide Proton), and Depiction of Copper(I) Nitrites and Copper(II) Nitrosyls, Where I−V Are Based on the DFT Results

blue microcrystals formed were filtered off. These microcrystals were redissolved in CH3CN, and ether diffusion to this solution yielded dark-greenish-blue needle-shaped crystals of 2 suitable for X-ray diffraction. The crystals were filtered off, washed with ether, and vacuum-dried (0.033 g, 68%). Elem anal. Calcd for C9H11N3O3SCu (2): C, 35.46; H, 3.64; N, 13.79. Found: C, 35.31; H, 3.48; N, 13.67. Selected IR frequencies (KBr disk, cm−1): 3022 (w), 2970 (w), 2934 (w), 2861 (w), 1615 (vs, νCO), 1595 (vs), 1569 (s), 1459 (m), 1407 (s), 1382 (s, νNO2), 1337 (m), 1266 (vs, νNO2), 1157 (m), 1096 (w), 1080 (w), 1035 (m), 1024 (m), 996 (w), 974 (w), 910 (w), 827 (w), 812 (w), 769 (s), 701 (w), 685 (m, νCS), 650 (m), 554 (w), 485 (w), 469 (w), 413 (w). Absorption spectrum [λmax, nm (ε, M−1 cm−1)]: in CH3OH, 262 (10232), 270sh (9840), 293 (7685), 355sh (2735), 613 (95); in CH3CN, 245 (16035), 265sh (12900), 303 (10400), 365sh (2477), 593 (125). 2.2.4. [(L2)Cu(CH3CO2)] (3). Method A. To a stirred solution of HL2 (0.10 g, 0.51 mmol) in 10 mL of methanol was added pinchwise solid NaH (0.013 g, 0.51 mmol). The solution color turned to light yellow. This light-yellow solution of NaL2 was added dropwise to a methanol solution (5 mL) of Cu(OAc)2·H2O (0.102 g, 0.51 mmol). The resulting dark-blue solution was stirred further for 4 h and kept for slow evaporation. After 1 week, dark-blue microcrystals obtained were filtered off, washed with ether, and vacuum-dried (0.112 g, 69%). Elem anal. Calcd for C11H14N2O3SCu (3): C, 41.57; H, 4.44; N, 8.81. Found: C, 41.46; H, 4.33; N, 8.76. Selected IR frequencies (KBr disk, cm−1): 3078 (w), 2970 (w), 2932 (w), 2854 (w), 1610 (vs, νCO), 1622 (vs, νa(COO)), 1594 (vs), 1569 (vs), 1407 (vs), 1338 (m), 1285 [vs, νs(CΟΟ)], 1265 (m), 1201 (m), 1100 (s), 1049 (m), 1023 (m), 995 (m), 811 (w), 757 (s), 684 (s, νCS), 649 (w), 621 (w), 555 (w), 448 (w). Absorption spectrum [λmax, nm (ε, M−1 cm−1)]: in CH3OH, 262 (11060), 270sh (10400), 298 (9175), 627 (155); in CH3CN, 245 (16980), 265sh (14870), 302 (11910), 610 (120). Method B. Complex 2 (0.050 g, 0.164 mmol) was dissolved in 10 mL of CH3OH. To the greenish-blue solution was then added glacial acetic acid (0.394 g, 0.656 mmol). The color of the solution changed from greenish-blue to blue, and the solution was stirred for 4 h and kept for slow evaporation. After 2 weeks, blue microcrystals that precipitated out were filtered off, washed with ether, and dried (0.038 g, 72%). 2.2.5. [Co(Cp)2][(L2)Cu(NO2)(CH3CN)] (4). The synthesis of this complex was performed inside a glovebox under a N2 atmosphere using dry degassed (freeze−pump−thaw) solvents. To a stirred greenish-blue solution of 2 (60 mg, 0.197 mmol) in a mixed solvent of 6 mL of CH2Cl2 plus 0.5 mL of CH3CN was added dropwise a 4 mL of CH2Cl2 solution of Co(Cp)2 (38 mg, 0.201 mmol). The solution color changed to brownish-yellow, the solution was stirred for 45 min, and then 25 mL of hexane was layered on top of the reaction mixture. After 4−5 h, the microcrystalline solid that precipitated out was filtered, washed with hexane, and dried (85 mg, 81%). The isolated solid was hygroscopic in nature. Selected IR frequencies (KBr disk, cm−1): 3435 (vs, νOH), 3106 (m), 2920 (w), 2840 (w), 2126 (w, br, νCN of CH3CN), 1615 (vs, νCO), 1590 (s), 1568 (s), 1440, (m), 1411 [s, νa(NO2)], 1370 (m), 1346 [w, νs(NO2)], 1275 (s), 1103 (w), 1060 (w), 1010 (m), 875 (s), 817 (w, δONO), 774 (m), 696 (m), 620 [m, br, ρw(NO2)], 503 (w), 460 (s, νCuN(nitrite)). 1H NMR (400 MHz, CD3CN): δ 8.55 (1H, d, py proton), 8.07 (1H, d, py proton), 7.89 (1H, t, py proton), 7.49 (1H, m, py proton), 5.21 (1H, s, Cp proton), 4.77 (3H, s, Cp proton), 3.56 (2H, t, −CH2CH2− proton), 2.74 (2H, t, Cp proton), 2.70 (2H, t, −CH2CH2− proton), 2.31 (4H, s, Cp proton and 8H impurity), 2.13 (3H, s, −SCH3), 2.09 (1H, s, acetone impurity), 1.96 (s, 3H, CH3CN). Crude Product (n-Bu4N)[(L2)Cu(NO2)]. The synthesis was performed under argon using a Schlenk line in degassed (freeze−pump− thaw) CH3CN. To a stirred CH3CN solution (8 mL) of the ligand HL2 (50 mg, 0.256 mmol) was added solid NaH (7.5 mg, 0.31 mmol). A light-yellow solution was generated. To this solution was then added solid [Cu(CH3CN)4](ClO4) (110 mg, 0.257 mmol). Immediately, the color changed to red, at which time the solution was stirred for 10 min and then to it was added solid (n-Bu4N)NO2 (75 mg, 0.26 mmol).

pyridine solution (10 mL) of picolinic acid (1.0 g, 8.13 mmol) was added dropwise a pyridine solution (2 mL) of 2-(methylthio)ethylamine (0.741 g, 8.13 mmol). The reaction mixture was stirred at 70 °C in an oil bath for 30 min. To this solution was added triphenylphosphite (2.52 g, 8.13 mmol) dropwise, the temperature was raised to 110 °C, and the resulting solution was stirred for 12 h. Pyridine was removed using a rotary evaporator. The yellow oil was dissolved in 50 mL of CHCl3 and washed with distilled water (3 × 100 mL), then with 100 mL of a brine solution, and again with water (2 × 100 mL). The organic layer was dried with anhydrous Na2SO4, and then CHCl3 was removed using a rotary evaporator, resulting in a light-yellow liquid (1.021 g, 64%). Elem anal. Calcd for C9H12N2OS (HL2): C, 55.07; H, 6.16; N, 14.27. Found: C, 54.96; H, 6.11; N, 14.12. Selected IR frequencies (KBr disk, cm−1): 3366 (s, νNH), 3058 (w), 2918 (w), 2850 (w), 1664 (vs, νCO), 1591 (s, νCN), 1528 (vs), 1500 (w), 1489 (m), 1466 (m), 1435 (m), 1363 (w), 1289 (w), 1266 (w), 1243 (s), 1199 (w), 1163 (m), 1089 (w), 1071 (w), 1024 (w), 979 (w), 940 (s), 816 (w), 751 (s), 692 (s, νCS), 620 (m), 560 (w). 1H NMR (400 MHz, CDCl3): δ 8.57 (1H, s, amide NH), 8.21 (1H, d, pyridine ring proton), 7.85 (1H, t, pyridine ring proton), 7.21 (1H, m, pyridine ring proton), 6.90 (1H, d, pyridine ring proton), 3.71 (2H, t, −CH2CH2− proton), 2.78 (2H, t, −CH2CH2− proton), 2.17 (3H, s, SCH3 proton). ESI MS for {HL2 + 1H}+. Calcd: m/z 197.06704 (100%). Found: m/z 197.07 (100%). 2.2.2. [(L2)Cu(H2O)Cl] (1). To a stirred solution of HL2 (0.15 g, 0.765 mmol) in 30 mL of methanol was added solid NaH (0.019 g, 0.765 mmol). The solution color turned to yellow. This yellow solution of NaL1 was added dropwise to a stirred yellowish-green solution of anhydrous CuCl2 (0.103 g, 1.233 mmol) in 30 mL of methanol. The color changed to dark blue after the complete addition of the ligand solution. The solution was stirred for 16 h and then kept for slow evaporation. After 2 weeks, dark-blue block-shaped crystals of 1 obtained were filtered off, washed with ether, and vacuum-dried (0.196 g, 82%). Elem anal. Calcd for C9H13N2O2SClCu (1): C, 34.61; H, 4.19; N, 8.97. Found: C, 34.49; H, 4.05; N, 8.84. Selected IR frequencies (KBr disk, cm−1): 3420 (Br, νOH), 3066 (w), 3078 (w), 2970 (w), 2934 (w), 2859 (w), 1616 (vs, νCO), 1594 (vs), 1568 (s), 1540 (w), 1408 (s), 1338 (w), 1299 (w), 1268 (w), 1199 (w), 1177 (w), 1035 (w), 1027 (w), 999 (w), 966 (w), 813 (w), 758 (s), 685 (s, νCS), 649 (w), 613 (w), 560 (w), 486 (w). Absorption spectrum [λmax, nm (ε, M−1 cm−1)]: in CH3OH, 262 (12140), 270sh (11260), 300 (9215), 315sh (8660), 648 (195); in CH3CN, 245 (15650), 265sh (13040), 311 (10140), 620 (165). 2.2.3. [(L2)Cu(ONO)] (2). To a stirred solution of 1 (0.05 g, 0.160 mmol) in 8 mL of methanol was added solid NaNO2 (0.110 g, 1.60 mmol) all at once. The resulting reaction mixture was then stirred for 2 days, at which time the blue color changed to greenish-blue. Then the solution was kept for slow evaporation, at which time the greenishC

DOI: 10.1021/acs.inorgchem.7b02897 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry The color changed to brownish-yellow, the solution was stirred for 30 min, and then the solvent was removed completely to isolate a yellow solid. Selected IR frequencies (KBr disk, cm−1): 2016 (w, νCN of CH3CN), 1606 (νCO, s), 1583 (s), 1553 (m), 1517 (m), 1463 (s), 1376 (br, s), 1330 (w), 1313 (m), 1260 (vs), 1133 (s), 1084 (vs, νClO of ClO4 present as the impurity), 1017 (w), 917 (w), 877 (m), 844 (w), 810 (w), 751 (s), 697 (w), 620 (s), 554 (w), 497 (w), 457 (w), 420 (w). 2.3. Physical and Computational Methods. The Fourier transform infrared (FTIR) spectra of the ligand and complexes were recorded on a Thermo Nicolet iS10 spectrometer using KBr pellets in the range 4000−400 cm−1. The electronic spectra were recorded on an Agilent 8453 diode-array spectrophotometer. Elemental analyses were carried out on a PerkinElmer 2400 Series II CHNS analyzer. Electron paramagnetic resonance (EPR) spectra were recorded using a MiniScope MS 5000 Magnettech EPR spectrometer at 298 and 77 K. Electrospray ionization mass spectrometry (ESI MS) spectra were recorded on a Waters HAB213 spectrometer. 1H NMR spectra were recorded on a JEOL JNM ECS 400 spectrometer. Redox potentials were measured using a CHI 1120A potentiometer. For constantpotential electrolysis experiments, a platinum mesh working electrode was used and the solute concentration was kept at ∼1.5 × 10−3 M. The crystal structure of [(L1)Cu(ONO)] was reported previously.16 Crystals of 1, suitable for X-ray diffraction, were grown by the slow evaporation of a CH3OH solution of the complex, whereas crystals of 2 were grown by diffusing ether into a CH3CN solution of 2. Single-crystal intensity measurements for 1 and 2 were collected at 90(2) K with a Bruker Smart APEX II CCD area detector using Mo Kα radiation (λ = 0.71073 Å) with a graphite monochromator (for 1 and 2). The cell refinement, indexing, and scaling of the data set were carried out using the SAINT and Apex2 programs.18 All structures were solved by direct methods with SHELXS and refined by full-matrix least squares based on F2 with SHELXL.19 The positions of the Cbound H atoms were calculated assuming ideal geometry and refined using a riding model. Figures showing the displacement parameters were created using the program XP.20 Crystal data for complexes 1 and 2 are summarized in Table 1. Additional crystallographic data and refinement details are available in CIF format from CCDC. DFT calculations were performed using the Gaussian 09 program.21 Geometry optimizations were performed starting from the X-ray structural coordinates without symmetry restrictions. The B3LYP functional22 was employed together with LANL2DZ23 with effective core potentials (ECPs) for Cu, cc-pVDZ24 for N, S, and O, and 631G(d,p)25 for C and H as basis sets. Wave-functional-stability calculations were performed on all optimized calculations to confirm that they corresponded to the true ground states. Natural bond orbital (NBO) calculations were performed on the optimized structure using Gaussian 09 software with the B3LYP functional and LANL2DZ basis set.

Table 1. Data Collection and Structure Refinement Parameters for Complexes 1 and 2 formula MW cryst syst color space group a (Å) b (Å) c (Å) α (deg) β (deg) γ (deg) V (Å3) Z dcalc(g cm−3) θ range, deg μ (mm−1) F(000) reflns collected unique reflns no. of param R1 [I > 2σ(I)]a wR2 [I > 2σ]b GOF residual density (e Å

−3

)

1

2

C9H13N2O2SClCu 312.26 monoclinic blue P21/n 6.9053(8) 20.380(2) 8.6514(10) 90 98.6366(18) 90 1203.7(2) 4 1.723 3.1−27.5 2.195 636 9760 2716 (Rint = 0.0165) 154 0.0186 [2604 data] 0.0494 1.066 0.408

C9H11N3O3SCu 304.81 monoclinic blue-green dichroic P21/c 7.521(2) 9.699(3) 15.381(4) 90 93.511(3) 90 1119.8(5) 4 1.808 2.7−39.0 2.136 620 11931 2559 (Rint = 0.0199) 155 0.0252 [2375 data] 0.0646 1.053 0.758

R 1 = ∑||F o | − |F c ||/∑|F o |. ∑w[(Fo2)2]}1/2. a

b

wR 2 = {∑ [w(F o 2 − F c 2 ) 2 ]/

(Figure S4), respectively, comparable to that of the reported complex [(L1)Cu(ONO)].16 Similarly for the CuII-coordinated acetate anion of 3, νa(CO2) and νs(CO2) at 1622 and 1265 cm−1, respectively, are evident in its IR spectrum (Figure S5).16 The isolated solid of the copper(I) nitro complex 4 is hygroscopic, as displayed in its FTIR spectrum (Figure S6); a broad and strong band at 3435 cm−1 (sample the absorbed moisture during the making of KBr pellets) and a weak band at 2126 cm−1 correspond respectively to νOH of the absorbed H2O and νCN of CH3CN. A set of peaks at 1411 [νa(NO2)], 1370 [ν s (NO2 )], 817 [δ(ONO)], 620 [ρw(NO 2)], and 460 (νCuN(nitrite)) cm−1 correspond to the κ1-N-bound NO2− moiety, comparable to the reported16 copper(I) nitro complex of ligand HL1. Also, the crude product (n-Bu4N)[(L2)Cu(NO2)], isolated following a different synthesis procedure (vide supra), displayed IR peaks (Figure S6) similar to those of the reported crude complex (n-Bu4N)[(L1)Cu(NO2)] of the analogous ligand HL1.16 The 1+ oxidation state of copper (i.e., d10 Cu) in 4 was confirmed from the 1H NMR spectrum of 4, which displayed all of the proton signals within the range 1−10 ppm (Figure S7). The electronic absorption spectra of 1−3 were recorded in CH3OH and CH3CN (for spectral data, see Figures S8 and S9 and Table S1). Each spectrum of 1−3 in CH3CN exhibits a weak broad absorption band at 620, 593, and 610 nm, respectively, due to d−d transitions (Figure S9A). The intense absorptions observed at ∼300 and ∼260 nm (or less) are due to the intraligand n−π* and π−π* transitions, respectively (Figure S9B). When a CH3CN solution of 1 is titrated with a CH3CN solution of (n-Bu4N)NO2, a clean transformation of 1 to 2 is observed, as monitored by UV−vis spectroscopy (Figure S10). The spectral changes featured the isosbestic points at 747, 553, 425, 355, 294, and 275 nm,

3. RESULTS AND DISCUSSION Ligand HL2 was synthesized following a condensation reaction of pyridine-2-carboxylic acid with 2-(methylthio)ethylamine in pyridine and characterized by MS, 1H NMR, and FTIR spectroscopy (νNH at 3366 cm−1 and νCO at 1664 cm−1; Figures S1−S3). Deprotonation of HL2 in methanol using NaH, followed by reaction with CuCl2, readily forms 1. The addition of NaNO2 or (n-Bu4N)NO2 to a CH3OH or CH3CN solution of 1 afforded 2 in high yield. Complex 3 was synthesized either from reaction of a methanol solution of 2 with glacial acetic acid or from reaction of the deprotonated methanol solution of HL2 with Cu(OAc)2·H2O. The absence of νNH and the red-shifted νCO (1610−1616 cm−1 for 1−3 compared to 1664 cm−1 of the free ligand) confirms amidato N− ligation to CuII in 1−3. The IR spectrum of 2 displays strong bands at 1382 and 1266 cm−1, which correspond most possibly to antisymmetric and symmetric stretching frequencies [νa(NO2) and νs(NO2)] of the CuII-coordinated NO2− ion D

DOI: 10.1021/acs.inorgchem.7b02897 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry

Figure 2. Thermal ellipsoid plot (probability level 50%) of 1 (left) and 2 (right) with the atom labeling scheme.

demonstrating straight conversion of 1 → 2, not mediated via any intermediate product. The development of a band at 365 nm is due to the NO2−-to-CuII charge-transfer transition (see Figure S9B; the 335 nm band developed after the addition of NO2− to the NaL2 plus ZnII solution), thus confirming NO2− ligation to CuII. In the case of the enzyme, the water molecule is replaced by a NO2− ion, thus introducing nitrite to the catalytic cycle. X-ray structures of 1 and 2 revealed a distorted squarepyramidal (τ = 0.098)26 and an octahedral coordination geometry around the CuII ion, respectively (Figure 2). In 1, three donors of L2− occupy three sites of the square plane and the remaining two positions are occupied by an axial water molecule and an equatorial Cl−, trans to the amidato N− donor. The elongated Cu−Owater distance of 2.2549(11) Å is due to the pseudo-Jahn−Teller distortion, commonly observed for the d9 CuII ion, reported before.16,27 The X-ray structure of 2 features three donors of L2− in a meridional position, whereas two O atoms of the NO2− anion and the carbonyl O atom of another ligand (to propagate a polymeric chain structure) occupy the remaining three positions. The Cu II−Namide distances are shorter than the CuII−Npy distances (Table 2), indicating stronger coordination of amidato N− than pyridine N. Asymmetric κ2-O,O binding of the nitrite is observed in 2, with a short Cu−Oeq distance of 1.9846(14) Å and a relatively long Cu−Oax distance of 2.6042(16) Å. These distances are comparable to the corresponding distances of NO2− of [(L1)Cu(NO2)];16 however, an appreciable elongation, ∼0.1 Å, of the Cu−S bond [Cu−S bond for 2 = 2.3900(7) Å and for [(L1)Cu(NO2)] = 2.3004(12) Å] and slightly longer Cu−N distances in 2 are evident (Table 2), implying a weaker coordination of L2− than L1−. 3.1. Evidence of a Change in NO2− Coordination, κ2O,O → κ1-N. The X-ray structures of oxidized CuNiRs exhibit an asymmetric κ2-O,O binding of NO2− to CuII. It is believed that the CuI-NO2 species is the key reaction intermediate that eventually undergoes NO evolution in the presence of protons.4,5,8−10 Because the reduction of CuII to CuI is necessary for the catalytic NO 2 − → NO conversion, information on the CuII/I redox potential is important. The more anodic potential of the CuII/I redox couple means that the CuI state is more easily achievable. In fact, an anodic CuII/I potential in the range (+)170 to (+)280 mV versus NHE (i.e., −74 to +36 mV vs SCE) is reported for CuNiR enzymes, isolated from various sources.28 To understand the redox behavior of 1−3, the cyclic voltammetry (CV) of each was recorded in a CH3CN solution using the same cell setup. A three-electrode cell setup such as platinum, saturated calomel

Table 2. Selected Bond Lengths (Å) and Angles (deg) for Complexes 1 and 2 and Reported Corresponding Complexes of Analogous Ligand HL1 [(L2)Cu(H2O)Cl] (1) Cu1−N1 Cu1−N2 Cu1−S1 Cu1−Cl1 Cu1−O2

a

2.0199(12) 1.9427(11) 2.3604(4) 2.2479(4) 2.2549(11)

[(L1)CuCl]n16 Cu1−N1 Cu1−N2 Cu1−S1 Cu1−Cl1 Cu1−Cl1′a

1.984(3) 1.947(3) 2.2881(9) 2.2442(9) 3.1697(9)

N1−Cu1−N2 81.61(5) N2−Cu1−S1 85.18(3) S1−Cu1−Cl1 93.491(14) N1−Cu1−Cl1 98.05(3) N2−Cu1−Cl1 160.63(4) N1−Cu1−S1 166.50(3) [(L2)Cu(ONO)]n (2)

N1−Cu1−N2 83.36(11) N2−Cu1−S1 85.96(8) S1−Cu1−Cl1 92.65(4) N1−Cu1−Cl1 97.14(8) N2−Cu1−Cl1 172.12(9) N1−Cu1−S1 167.84(8) [(L1)Cu(ONO)], molecule 116

Cu1−N1 Cu1−N2 Cu1−S1 Cu1−O1Aa Cu1−O2 Cu1−O3

2.0293(15) 1.9319(15) 2.3900(7) 2.2947(13) 1.9846(14) 2.6042(16)

Cu1−N1 Cu1−N2 Cu1−S1

1.992(2) 1.930(2) 2.3004(12)

Cu1−O2 Cu1−O3

1.9759(19) 2.554(2)

N1−Cu1−N2 N2−Cu1−S1 S1−Cu1−O2 N1−Cu1−O2 O2−N3−O3 N1−Cu1−S1 N2−Cu1−O2

81.80(6) 84.78(4) 97.47(4) 94.46(6) 116.70(17) 161.70(4) 172.86(16)

N1−Cu1−N2 N2−Cu1−S1 S1−Cu1−O2 N1−Cu1−O2 O2−N3−O3 N1−Cu1−S1 N2−Cu1−O2

83.62(9) 87.05(7) 93.63(7) 95.21(8) 115.1(2) 168.27(6) 176.09(7)

Symmetry codes: A = −x, y − 1/2, −z + 1/2; ′ = x, y + 1, z.

electrode (SCE), and a platinum wire as the working, reference, and auxiliary electrodes, respectively, were used for measurement of the potentials. As expected, the CH3CN solution of 1 displays two reductive responses, one irreversible response at Epc = −0.30 V for CuII → CuI reduction and a quasi-reversible response at E1/2 = −0.67 V (Epc = −0.76 V; Epa = −0.58 V) corresponding to CuI → Cu0 reduction (Figure S11). Unlike the chloro-ligated complex 1, the cyclic voltammogram of the copper(II) nitrito complex 2 displays three irreversible reduction waves at Epc values of −0.32, −0.49, and −0.63 V, as shown in Figure 3A, attributed to the presence of NO2− coordination (instead of Cl−), which may undergo linkage isomerization to produce O- and N-bonded copper nitrite species. The first reduction that occurs at −0.32 V for 2 is due E

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→ Cu0, of the κ1-N-bound CuI-NO2− complex III (Scheme 2), indicating the absence of III at the working electrode surface. At such a high scan rate, the formed I does not find sufficient time to reorganize its NO2− binding to produce III. This flipping of the NO2− binding observed for 2 is much slower than that observed in the case of [(L1)Cu(ONO)].16 For 2, at 100 mV s−1 scan rate, the response at Epc = −0.49 V vanishes (Figure 3B), whereas for [(L1)Cu(ONO)], the scan rate required is 500 mV s−1. Because O is a stronger donor than N, the more cathodic response (Epc = −0.66 V) corresponds to I → [(L2)Cu0(κ2-ONO)]2− and the less cathodic response (Epc = −0.49 V) corresponds to III → [(L2)Cu0(κ1-NO2)(CH3CN)]2− reduction, as shown in Scheme 2. A similar linkage isomerization of NO2− is reported by Tanaka and coworkers,8d where a potential difference of 170 mV between two copper(I) isomers, one with κ1-O and the other with a κ1-Nbonded nitrite moiety, has been observed. A similar potential difference (CuI → Cu0 reduction) of 170 mV between I and III is evident (Scheme 2) from the CV measurement of 2. The CV profile of 2 (Figure 3A) similar to that of [(L1)Cu(ONO)] and the theoretical calculation explicitly agree to change of the NO2− coordination mode upon CuII → CuI reduction, which is strongly supported by the FTIR spectra of 4 and (nBu4N)[(L2)Cu(NO2)], both of which displayed δONO at ∼800 cm−1 and νCuN at ∼460 cm−1, as reported for the copper(I) nitro complex of HL1.16 Similar δONO and νCuN bands at 800 and 400 cm−1, respectively, are reported for a copper(I) nitro complex that is confirmed by the 15N-labeled CuI-15NO2− complex.9f 3.2. Evidence of NO Evolution. To check whether a oneelectron-reduced species of 2 produces NO in the presence of protons, a CH3CN solution of 2 was electrolyzed by applying a constant potential of −0.42 V. The electronic absorption spectral changes that occur during electrolysis are shown in Figure 5A. The disappearance of the d−d band at 593 nm confirmed the complete reduction of CuII → CuI and, hence, formation of the intermediate CuI-NO2 species. The amidato N− of deprotonated HL2 has a strong σ-donor ability that ensures its binding to both the CuII and CuI states and enables a check on the acid response of this reduced species. When 2.2 equiv of CH3CO2H was added to the reduced solution of 2 and CV scans were performed, an abrupt increase of the current height at Epc = −0.93 V was observed, as shown in Figure 5B. After a maximum current height is reached, the response at Epc = −0.93 V starts to decrease because of NO loss from the bulk solution to the headspace of the coulometry cell. This potential at Epc = −0.93 V corresponds to the reduction potential of free NO(g)30 that is generated in situ from the reaction 2− + 2CH3CO2H → NO(g) + 3 + H2O. From the calibration curve (Ιmax (μA) vs [NO] in ppm; Figure S16), ∼97% NO evolution was observed. This huge current height at Epc = −0.93 V vanishes when the CV scan is performed after purging the solution with argon gas (Figure 5B, red e trace). This indicates that the response at Epc = −0.93 V is due to the reduction of a gaseous product that easily escapes from the bulk solution when argon is purged. This released gas is allowed to react anaerobically with a CH2Cl2 solution of [Co(TPP)], which readily generates [Co(TPP)NO],31,9i characterized by UV−vis (Soret and Q bands at λmax = 414 and 536 nm, respectively; Figure S17) and FTIR (after removal of CH2Cl2, the solid obtained displays νNO at 1693 cm−1; Figure S18) spectroscopy, thereby confirming its identity as NO. The final CV achieved (red trace e in Figure 5B) is the same as that of 3, thus

Figure 3. Cyclic voltammograms of 2 in CH3CN containing 0.1 M [(n-Bu)4N]ClO4 as the supporting electrolyte at 298 K at a platinum working electrode using SCE as the reference electrode (A) at a scan rate of 30 mV s−1 and (B) at various scan rates (30, 40, 50, and 100 mV s−1) showing κ2-O,O → κ1-N flipping of NO2− binding.

to the CuII → CuI conversion (red trace, Figure 3A); the reverse scan from −0.42 V toward 0.0 V does not show any response that corresponds to the stripping potentials, characteristic of the Cu0 → Cu1 reoxidation that occurs with high current intensity.29 However, a stripping potential of −0.22 or −0.18 V is observed when the scans have been performed beyond the second (blue trace) or third reduction (black trace) waves of Epc = −0.49 and −0.63 V, respectively. These two reductions at higher cathodic potentials are therefore due to the CuI → Cu0 reduction of two different CuI species generated in situ in the solution: one is most possibly [(L2)CuI(NO2)]−, and the other is [(L2)CuI(ONO)]−, having κ1-N- and asymmetric κ2-O,O-bound NO2− respectively. To check whether the speculated coordination isomerization of NO2− is energetically favorable, we performed DFT calculations using the B3LYP functional22 on various CuI-NO2− models like [(L2)CuI(κ2-ONO)]− (I), [(L2)CuI(κ1-NO2)]− (II), and [(L2)CuI(κ1-NO2)(CH3CN)]− (III), as shown in Figure 4

Figure 4. DFT-optimized structures of CuI-NO2− with a κ2-O,O- and κ1-N-bound NO2− ion, where Er = relative energy of I−III, considering the absolute energy of II to be zero and the Cu−S distance of the corresponding structures.

(see Figures S12−S15 for bond distances, atomic composition, and the HOMO and LUMO energies for 2 and I−III). The DFT-optimized structures revealed that nearly tetrahedral (Td) I is slightly less in energy (2.6 kcal mol−1) than the tricoordinate CuI complex II but much higher in energy than the Td CuI species III (III is 10.9 kcal mol−1 less in energy than I); therefore, the transformation I → II is unfavorable, but I → III is highly favorable in the CH3CN medium, corroborating the energetically promising κ2-O,O → κ1-N transition of NO2− binding. Such changes of the NO2− coordination require time; therefore, the CV trace taken at high scan rate such as above 100 mV s−1 reveals the disappearance of the response at Epc = −0.49 V (Figure 3B, red), which corresponds to reduction, CuI F

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Scheme 2. Chemdraw Depiction of Switching the NO2− Binding Mode upon CuII → CuI Reduction (Potentials Are vs SCE and for 2)

Figure 5. (A) Electronic absorption spectral changes during coulometric reduction of a CH3CN solution of 2, showing 2 → 2− (black → red trace) conversion. (B) Cyclic voltammograms in CH3CN containing 0.1 M [(n-Bu)4N]ClO4 as the supporting electrolyte at 298 K at a platinum working electrode at a scan rate of 300 mV s−1 using SCE as the reference electrode of 2 (1.093 mM solution, black trace, i.e., a), gradual development of the −0.93 V response after the addition of CH3CO2H (green → blue → pink i.e. b → c→d traces) and then after purging argon gas for 2−3 min, showing the escape of NO(g) from solution when the −0.93 V response is absent (red trace e).

confirming the reaction as 2− + 2CH3CO2H → NO(g) + 3 + H2O. 3.3. Evidence of Copper(II) Nitrosyl Formation. To assess whether NO generation occurs through a {CuNO} intermediate, the following experiments are executed. When a CH3CN solution of 2 is electrolyzed at −0.42 V, an abrupt decrease of the 593 nm band is observed, which indicates rapid formation of the corresponding CuI-NO2 species (red trace in Figure 5A and cyan trace in Figure 6). This coulometrically reduced solution was cooled to −40 °C, and the electronic spectrum was recorded immediately after the addition of CH3CO2H. Remarkably, the spectrum obtained after acid addition (red trace, Figure 6) features two distinct lower-energy bands, each attributed to a d−d transition, one at 722 nm and the other at 610 nm, of which the former is assumed to be due to the in situ formed, highly unstable copper(II) nitrosyl species and the latter corresponds to that of 3. In fact, the next scan, taken within 15 s, surprisingly displays no band at 722 nm but retains the 610 nm band with an increased intensity that matches to the d−d band of 3 (blue trace, Figure 6). The 722 nm band indicates that the species in situ generated is a copper(II) species but not a copper(I) species or 2 or 3; those display either no d−d band or a d−d band at 593 or 610 nm, respectively, as shown in Figure 6. This lower-energy absorption at 722 nm is comparable to that of a reported copper(II) nitrosyl intermediate, obtained from the reaction of

Figure 6. Electronic absorption spectra in CH3CN at −40 °C of 2 (black), electrochemically reduced 2− (cyan), 2− + CH3CO2H taken immediately (red), and the same solution after 15 s (blue), showing {CuNO} → 3 transformation. i

[( Pr3tacn)CuI(NO2)] with an organic acid, that displays a d−d band at 680 nm.9e However, authors have reported their doubt on whether the 680 nm band is of the copper(II) nitrosyl formed or of the final acetate-bound copper(II) complex, [(iPr3tacn)Cu(CF3CO2)2], that displayed a d−d band at 692 nm, close to 680 nm. To the best of our knowledge, no other CuII/I-NO2− model is reported that has been shown to generate G

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Figure 7. X-band EPR spectra measured at 77 K in a CH3CN solution (A) of 2 (red trace), a reduced solution of 2 (green), a reduced solution of 2 plus CH3CO2H (black trace; underneath this black trace are three other spectra, each taken at 5 min intervals, shown in the inset after enlargement), the frozen solid dipped in a −40 °C bath to melt, and then a spectrum taken at 77 K (blue trace). (B) Spectra taken following the same processes as above but with [(L1)Cu(ONO)] instead of 2. Spectrometer settings: microwave frequency = 9.416 GHz; power = 10 mW; modulation frequency = 100 kHz; modulation amplitude = 5 G.

copper(II) nitrosyl, characterized by UV−vis spectroscopy.8 Tolman et al. have also reported similar instability of copper(II) nitrosyl species, generated from a CuI-NO2 precursor, followed by organic acid treatment, that immediately transforms to the more stable complex with a bound conjugate base of the acid used, even at −80 °C, showing no evidence of copper(II) nitrosyl in its electronic spectrum.9c Quite interestingly, Mondal et al. have reported the formation of a copper(II) nitrosyl that is stable at room temperature for a few hours, exhibiting a d−d transition at 645 nm.32 The reported structurally characterized copper(II) nitrosyl, [Cu(CH3NO2)5(NO)](PF6)2, displays a band at 819 nm, much lower in energy than any other copper(II) nitrosyl species reported so far.13 Exactly the same experiment with complex [(L1)Cu(ONO)], instead of 2, designates no formation of copper(II) nitrosyl but rather indicates the formation of [(L1)Cu(CH3CO2)] like other reported models of CuNiR.8 The coplanarity of ligand donors and conjugation of L1− (compared to L2−) is expected to stabilize the CuII state with CH3CO2− rather than with a neutral NO radical, therefore promptly producing the complex [(L1)Cu(CH3CO2)] via [(L1)CuII(NO)]+. We believe that the copper(II) nitrosyl formed is of the {CuNO}10 type, which can be formulated as CuII-NO• or CuINO+. The most reliable way to check it is by EPR spectroscopy. Regardless of the description either as CuI-NO+ or as CuIINO•, both will be EPR-silent because the former has no unpaired spins, whereas the latter exhibits strong antiferromagnetic coupling of the two unpaired spins (one on CuII and the other on •NO) at low temperature, resulting in an St = 0 ground state. Complex 2 in a CH3CN solution at 77 K displays a strong EPR signal at g = 2.09 with weak copper hyperfine splitting, marked as red vertical lines (red trace, Figure 7A). The electrochemically reduced solution of 2 should be EPRinactive; however, it exhibits a weak signal at g = 2.09 (green trace, Figure 7A) at 77 K. This weak signal is due to the minute amount (5.5%; Figure S19) of copper(II) species formed during electrolysis via the disproportionation reaction 2CuI → Cu0 + CuII. Similar weak EPR signals are reported for other CuI-NO2 models.9f,13 The reduced CH3CN solution of 2 was then cooled to −40 °C (the freezing point of CH3CN is −45 °C, ensure quick freezing of a solution precooled at −40 °C), and to it was added CH3CO2H. Immediately the sample tube was dipped

into liquid N2, and the EPR spectrum was recorded; it showed a signal of intensity (black trace, Figure 7A) similar to that of the reduced form of 2 (green trace, Figure 7A). The enlarged spectrum (black trace, inset of Figure 7A) indicates an axial spectral profile with g∥ = 2.26 and g⊥ = 2.08 and a Cu hyperfine splitting, A∥Cu = 16 mT, that is the same as that of 3 but unlike that of the reduced solution that displayed an isotropic signal at g = 2.09 (Figure S20). This indicates that the copper(II) species generated via disproportionation reacts rapidly with an acetate anion to form 3. The same intensity of the EPR signal (green and black traces, Figure 7A) clearly states that either no reaction of acid with a reduced solution of 2 occurred or maybe an EPR-silent species is formed. The former reason can be discarded based on the low-temperature (−40 °C) UV−vis spectral results, which revealed different spectra for the reduced 2 (cyan trace, Figure 6) and the reduced 2 plus CH3CO2H solution (red trace, Figure 6). Therefore, the latter reason seems judicious; i.e., a transient species is formed that is EPRsilent. While keeping the sample at 77 K, three more spectra were recorded, each at 5 min intervals, to check for further changes. The successive spectra taken show very few changes, almost overlaid on each other (Figure 7A, inset, and Figure S20). This small change most possibly is due to the NO loss and subsequent formation of 3 even at 77 K, thus firmly supporting that the copper(II) nitrosyl formed is of the {CuNO}10 type, which is EPR-silent, quite stable at 77 K, and undergoes NO loss very slowly to produce 3. Next, the sample tube containing the frozen sample was taken out of the liquid N2 and dipped into a −40 °C isopropyl alcohol bath. Just after melting, it was dipped again into liquid N2, and the EPR spectrum was recorded that displayed an intense signal similar to that of 3, indicating that [(L2)CuII(NO)]+ at −40 °C rapidly evolves NO and subsequently reacts with an acetate anion to form stoichiometric 3. In the context of the EPR-silent behavior of the copper nitrosyl species, it is worth mentioning here the interesting phenomenon observed first by Tolman and co-workers.33 With a structurally characterized {CuNO}11 model complex, TptBuCuNO, considering isotope-labeled NO (14NO and 15 NO), they showed that, because of very fast spin relaxation, this {CuNO}11 species surprisingly did not exhibit a EPR signal at 77 K, although it has an EPR-active S = 1/2 ground state. However, the same species below 40 K displays a EPR signal (as expected for an S = 1/2 system) with considerable hyperfine H

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to obtain the stability order of five- versus four-coordinate nitrosyl species in both spin states (SS and TS). An energy ordering such as VTS < VSS < IVSS < IVTS is observed from the DFT calculations (Figure S23). The energy differences of each consecutive pair of structures starting from VTS are 11.71, 8.64, and 0.06 kcal mol−1. In VSS, IVSS, and IVTS, the amidato N− is seen to be trans to NO, which may facilitate NO release because of the trans labialization effect. Regardless of the spin states of IV, the equatorial position of NO remains unchanged (Figures S21 and S22); however, in the case of V, interchange of the coordination position between CH3CN and NO occurs (Figures 8 and S24 and S25) upon changing spin states. It is

coupling details at g ∼ 2.0. Therefore, without measurement of the EPR spectrum at much lower temperature than 77 K, it is not possible to determine with certainty whether the copper nitrosyl formed is of the {CuNO}10 or {CuNO}11 type. The other complementary way that assists the assignment of such copper nitrosyl species is measurement of the electronic absorption spectrum at low temperature; the {CuNO}11 species does not display the lower-energy d−d absorption band, whereas the {CuNO}10 species does. The observation of 722 nm absorption at −40 °C (233 K) for the present case thus strongly supports that the copper nitrosyl formed is of the {CuNO}10 type. The extra feature seen in the final EPR spectrum (blue trace, Figure 7A) is the existence of two additional peaks that coincide with those of 2, as marked with vertical red lines. Solomon et al. have shown that both (i) the reaction of a substoichiometric NO(g) solution (10:1, enzyme/NO) with reduced NiR and (ii) the reaction of NO(g) with oxidized NiR produce T2 CuII-NO2− species, as is evident from EPR spectroscopic measurement (Figure 2, red traces, in ref 34).34 In the presence of excess NO(g), the copper(I)-mediated disproportionation, CuI + 3NO → N2O + NO2− + CuII, may generate NO2− anion and hence CuII-NO2−.11b,34 In the present case when the frozen solution was kept at −40 °C to melt, a sudden release of NO(g)35 from [(L2)CuII(NO)]+ may react with (i) the remaining [(L2)CuII(NO)]+ that does not yet release NO to form [(L2)CuII(solv)]+ or (ii) [(L2)CuII(solv)]+ that does not yet transform to 3; thereby, CuII → CuI reduction and another molecule of NO association and disproportionation via a dinitrosylcopper(I) intermediate is possible that finally leads to the formation of CuII-NO2− species, as proposed by Solomon et al.34 Therefore, the blue trace of Figure 7A is the spectrum of a mixture of mostly 3 and a minute amount of 2. The EPR spectrum of [(L1)Cu(ONO)] is reported.36 Following the same process of EPR spectral acquisition probing [(L1)Cu(ONO)] instead of 2 revealed that all of the spectra (black, blue, and red traces in Figure 7B), except that of the reduced species (green trace, Figure 7B), display a strong signal of almost the same intensity and spectral profile with three principal g values at 2.20, 2.05, and 1.99, unlike the reduced species, which is much less intense. This observation indicates that the [L1)Cu(NO)]+ → [(L1)Cu(CH3CO2)] transformation is very fast at −40 °C; it does not allow us to capture [L1)Cu(NO)]+ even if we immediately dip the precursor solution (reduced [(L1)Cu(ONO)] plus CH3CO2H) into liquid N2. 3.4. DFT Calculation on Modeled Copper(II) Nitrosyls. To gain information on the structure and bonding, DFT calculations on the modeled copper(II) nitrosyls such as [(L2)Cu(NO)]+ (IV) and [(L2)Cu(NO)(CH3CN)]+ (V) considering both singlet-state (SS) and triplet-state (TS) electronic configurations were performed at the B3LYP level using the basis set for various atoms, as mentioned in section 2.3, and the corresponding structures are denoted as (IV or V)SS or TS. With the present ligand system, CuII likely prefers more than four coordination (Figure 2); therefore, to obtain an energy-optimized structure of IVSS, the side-on NO binding was considered, anticipating a five-coordinate complex along with tridentate L2− ligation. The energy-optimized structure, however, revealed an end-on N coordination of NO to CuII (Figures S21 and S22), adopting a four-coordinate squareplanar geometry around copper. Therefore, the five-coordinate model V with an additional CH3CN molecule was considered

Figure 8. DFT-optimized structures of VSS (top) and VTS (bottom) and their HOMOs. Color code: C, black; N, blue; O, red; S, yellow; H, pearl; Cu, light orange. Atomic composition for HOMO (LUMO) of VSS (%): 6 (21), Cu; 6 (34), NNO; 4 (19), ONO; 43 (5), Namide; 24 (2), Oamide. Atomic composition for HOMO (LUMO) of VTS (%): 2 (1), Cu; 36 (36), NNO; 59 (62), ONO; 1 (0), Namide; 1 (0), Oamide. DFTcalculated and corrected (calculated values are multiplied with a scaling factor of 0.952) FTIR stretching frequencies of copper(II)coordinated NO (νNO) and the CH3CN (νCN) molecule are mentioned below the structures VSS/TS.

noteworthy that VTS shows axial NO ligation with a significantly long Cu−N(NO) distance of 2.948 Å, revealing almost no bonding of NO to CuII. Therefore, the energetically favorable spin-state change, SS → TS, in V may be envisioned to form an adduct of [(L2)CuII(CH3CN)] and •NO, thus explaining easy NO loss, a unique information. Also for VTS, more than 95% contribution of NO atomic orbitals to both HOMO and LUMO indicates that NO-centered oxidation and reduction may occur. Therefore, the NO moiety present here is as •NO, for which oxidation to ON+ and reduction to NO− are feasible, consistent with its formulation as CuII-NO•. The NBO calculation on optimized IVSS/VSS further supports this formulation, indicating copper in the 2+ oxidation state [IV core, 4S(0.35)3d(9.56)4p(0.36); V core, 4S(0.35)3d(9.54)4p(0.54)]. The DFT calculation revealed a crucial role of CH3CN ligation that eventually assists to release NO. The Cu− N(NO) and N−O distances and the Cu−N−O angle of VSS/TS I

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Inorganic Chemistry are shown in Figure 8, and the corresponding values for IVSS/TS are 1.963 Å, 1.140 Å, 121.51° and 2.150 Å, 1.146 Å, 147.49°, respectively. These metric parameters for both IVSS and VSS are close to the corresponding values of 1.955(4) Å, 1.109(5) Å, and 121.0(3)°, respectively, of the structurally characterized complex13 [Cu(CH3NO2)5(NO)](PF6)2 and to its DFToptimized structure.12 The calculated IR spectra of all of the nitrosyl models, (IV/ V)SS/TS, are shown in Figures S26−S29. To get the fundamental mode vibrational frequencies of a copper-coordinated NO moiety, the calculated frequencies were multiplied with a suitable scaling factor37 of 0.952, which indicates the νNO values of the IVSS, IVTS, VSS, and VTS models as 1801, 1917, 1802, and 1904 cm−1, respectively, which are comparable to the experimentally obtained reported νNO values.13,32a For example, the structurally characterized {CuNO}10 complex, [Cu(CH3NO2)5(NO)](PF6)2, in both solution and solid state exhibits νNO at 1933 cm−1, showing easy NO loss under vacuum,13 whereas Mondal and co-workers reported νNO at 1846 cm−1 for a copper(II) nirosyl species.32a Furthermore, the models VSS and VTS display νCN of copper-coordinated CH3CN at 2262 and 2280 cm−1, respectively. The relative positions and intensity variations of νNO and νCN of VSS and VTS are in good agreement with the calculated structure (weaker CH3CN and stronger NO coordination in VSS than VTS) presented in Figure 8. We have also performed the calculation on models VSS/TS, considering an adequate basis set such as 6-311G(d,p) for all atoms that revealed quite similar geometries, IR frequencies, and absolute energies (ΔE of VTS/VSS = 10.63 kcal mol−1) but different structural parameters, as shown in Figures S30−S32.

Accession Codes

CCDC 1567068−1567069 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.

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*E-mail: [email protected]. ORCID

Marilyn M. Olmstead: 0000-0002-6160-1622 Apurba K. Patra: 0000-0001-7232-1274 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank the Science Engineering and Research Board (SERB), Government of India (GOI), for financial support (Grant EMR/2014/001059), DST-FIST, GOI, for providing basic infrastructural facilities (Grant SR/FST/CSI-267/2015), and Alexander von Humboldt Foundation, Germany, for an equipment donation grant of a spectroelectrochemical analyzer. R.C.M. thanks the University Grants Commission for a fellowship. We sincerely thank Prof. R. Mukherjee, IIT Kanpur, for his assistance. The reviewers’ suggestions are highly acknowledged.

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4. CONCLUSIONS In summary, the copper(II) complexes supported by a monocarboxamide N2S donor ligand have been synthesized and characterized. Complex 2 exhibits many important aspects of the nitrite reduction pathway, parallel to CuNiR, such as (i) ready conversion of 1 + NO2− → 2, (ii) an X-ray structure of 2 that reveals asymmetric κ2-O,O binding of NO2−, (iii) electrochemical reduction of 2 that produces intermediate CuI-NO2 species, (iv) NO2− binding mode conversion, κ2-O,O → κ1-N, (v) formation of a copper(II) nitrosyl intermediate in the presence of a proton, (vi) DFT calculation on modeled copper(II) nitrosyls that supports end-on N coordination of NO to CuII, (vii) equivalent NO generation, and, most remarkably (viii) NO formation via the copper(II) nitrosyl species. To the best of our knowledge, 2 is the first example of a CuII-NO2− that exhibits copper(II) nitrosyl formation prior to NO evolution, supporting the route I mechanism. Also, theoretical evidence of easy NO loss due to spin-state changes of copper(II) nitrosyl species (VSS → VTS) is unique. This information sheds new light on copper-mediated nitrite reduction to NO.

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AUTHOR INFORMATION

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REFERENCES

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