The dinitrosyliron complex [Fe4(μ3-S) 2(μ2-NO)2(NO)6]2- containing bridging nitroxyls: 15N (NO) NMR analysis of the bridging and terminal NO-coordinate ligands

Article abstract of DOI:10.1039/c4dt00450g

The fluxional terminal and semibridging NO-coordinate ligands of DNIC [Fe₄(μ₃-S)₂(μ₂-NO) ₂(NO)₆]^2-, a precursor of Roussin's black salt (RBS), are characterized by IR ν(NO), ¹⁵N (NO) NMR and single-crystal X-ray diffraction. the Partner Organisations 2014.

Full text of DOI:10.1039/c4dt00450g

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The dinitrosyliron complex [Fe4(μ3-S)2-
(μ2-NO)2(NO)6]2− containing bridging nitroxyls:
Cite this: Dalton Trans., 2014, 43,
9022
15N (NO) NMR analysis of the bridging and
Received 14th February 2014,
Accepted 23rd April 2014
terminal NO-coordinate ligands†
DOI: 10.1039/c4dt00450g
Shih-Wey Yeh, Chih-Chin Tsou and Wen-Feng Liaw*
www.rsc.org/dalton
The fluxional terminal and semibridging NO-coordinate ligands of conditions.1b In this report, the complex [Fe4(μ3-S)2(μ2-NO)2-
DNIC [Fe4(μ3-S)2(μ2-NO)2(NO)6]2−, a precursor of Roussin’s black (NO)6]2− (1) with semi-bridging nitroxyls acting as a key
salt (RBS), are characterized by IR ν(NO), 15N (NO) NMR and single- intermediate in the transformation of RRS into RBS via the
crystal X-ray diffraction.
assembling process RRS → complex 1 → RBS was reported.
The IR ν(NO) and 15N (NO) NMR spectra implicate that
complex 1 is fluxional, scrambling terminal and bridging NO
ligands at 320 K. In particular, the 15N (NO) NMR chemical
shift serving as an efficient tool to discriminate terminal and
bridging NO-coordinate ligands was demonstrated.
Nitric oxide has been identified as a signaling molecule parti-
cipating in diverse physiological functions through interaction
with NO-responsive targets.1 Iron–sulfur clusters [Fe–S] were
known to be the pivotal prosthetic groups targeted by NO.2
The reported nuclear resonance vibrational spectroscopy
(NRVS) and EPR-spectroscopic studies reveal that the major
products in nitrosylating specific [Fe–S] proteins are the dia-
magnetic species, e.g. Roussin’s red ester (RRE), Roussin’s red
salt (RRS) or Roussin’s black salt (RBS), in addition to the di-
nitrosyliron complex (DNIC) with a characteristic EPR signal
gav = 2.03.3 Also, RBS was characterized as the predominant
product upon adding NO to a mutant [4Fe–4S] ferredoxin from
Pyrococcus furiosus by using NRVS.3b Recently, on the basis of
resonance Raman and low-temperature photolysis FTIR data,
the diferrous site of an FMN-free FDP (flavodiiron protein)
from Thermotoga maritima (Tm deflavo-FDP) triggering the
turnover of 2NO to N2O via a NO-semibridging FeII(μ-NO)FeIII
intermediate was proposed.4 In the synthetic model, {Fe-
(NO)2}9 thiolate-containing DNICs converted back to [4Fe4S]
The reaction of [Fe2(μ2-S)2(NO)4]2− with two equiv. of {Fe-
(NO)2}10 DNIC [(TMEDA)Fe(NO)2] (TMEDA = tetramethylethyle-
nediamine) in CH3CN afforded [Fe4(μ3-S)2(μ2-NO)2(NO)6]2− (1)
bearing bridging and terminal NO ligands, characterized by
IR, UV-vis, SQUID, 15N NMR and single-crystal X-ray diffraction
(Scheme 1a). The reaction is presumed to proceed via coordi-
native association of [(TMEDA)Fe(NO)2] and RRS accompanied
by release of the labile TMEDA ligand. The straightforward
conversion of RRS into complex 1 was monitored by the IR
νNO (1742 w, 1701 s and 1668 m cm−1 (CH3CN)). With the
aid of isotopic labeling experiments, the reaction of CH3CN
solutions of [(TMEDA)Fe(15NO)2] and [Fe2(μ2-S)2(14NO)4]2−
in
a 2 : 1 molar ratio yielded semi-enriched [Fe4(μ3-S)2-
(14NO)4(15NO)4]2− (1-15NO) identified by the characteristic
IR νNO spectrum (νNO: 1721 br, 1685 sh, 1657 vs, 1638 sh, 1510 w
and 1483 m cm−1 (KBr)), compared to νNO (1739 w, 1702 sh,
1685 vs, 1668 s and 1510 m cm−1 (KBr)) for complex 1 (ESI
Fig. S1†). The magnitude of ∼27 cm−1 of the isotopic shift
clusters via reassembling processes (DNIC
→ RBS →
[Fe4S4(NO)4]2− → [4Fe–4S] cluster) and the transformation of
{Fe(NO)2}9 DNICs into [2Fe2S] clusters mediated by RRS were
demonstrated.5 In contrast to the inertness of [Fe2(μ2-S)2-
(NO)4]2− (RRS) toward alkaline medium, RRS readily trans-
forms into the various polynuclear clusters ([Fe4(μ3-S)3(NO)7]−
(RBS), [Fe5(μ3-S)4(NO)8]−, and [Fe7(μ3-S)6(NO)10]−) via the pro-
posed protonated intermediate [Fe2(μ2-SH)2(NO)4] under acidic
Department of Chemistry, National Tsing Hua University, Hsinchu 30013, Taiwan.
E-mail: wfliaw@mx.nthu.edu.tw; Fax: +886-3-5711082;
Tel: +886-3-5715131 ext 35663
†Electronic supplementary information (ESI) available: Experimental details,
crystal data, computational details, SQUID, cyclic voltammogram, and IR.
CCDC 974703. For ESI and crystallographic data in CIF or other electronic
format see DOI: 10.1039/c4dt00450g
Scheme 1 Conversion pathway from RRS to RBS via complex 1.
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Fig. 2 Molecular structure of complex 1. Selected bond distances (Å)
and angles (°): Fe(1)⋯Fe(2) 2.573(1); Fe(1)⋯Fe(1i) 2.740(1); K(1)⋯O(2)
2.777(3); Fe(1)–N(1) 1.660(3); Fe(1)–N(2) 1.761(3); Fe(2)–N(2) 1.967(3);
Fe(2)–N(3) 1.676(4); N(1)–O(1) 1.184(4); N(2)–O(2) 1.224(4); N(3)–O(3)
1.182(5); N(4)–O(4) 1.181(4); Fe(1)–N(1)–O(1) 170.2(3); Fe(1)–N(2)–O(2)
138.8(3); Fe(2)–N(2)–O(2) 131.0(3).
Fig. 1 15N NMR spectra of complex 1 in d6-acetone at (a) 320 K,
(b) 300 K, (c) 250 K and (d) 220 K, respectively.
Fig. 2 and selected bond dimensions are presented in the
figure caption. The molecule is symmetrical because of a crys-
from 1510 cm−1 (μ-NO) to 1483 cm−1 (μ-15NO) is consistent tallographically imposed inversion center. The unique ladder-
with the calculated position, based only on the difference in shaped structure is constructed from one RRS [Fe2(μ-S)2(NO)4]
mass between 14NO and 15NO.5c The IR ν(NO) spectra suggest moiety coordinated by two [Fe(NO)2] motifs. The Fe(1)⋯Fe(1i)
that complex 1 is fluxional, scrambling terminal and bridging distance of 2.740(1) Å is longer than the Fe⋯Fe bond distance
NO ligands at room temperature. This point has received of RRS (2.678 Å), and the relatively short Fe(1)⋯Fe(2) distance
further support from the study of temperature-varied 15N NMR of 2.573(1) Å suggests stronger Fe⋯Fe interaction. The brid-
of complex 1. As shown in Fig. 1a, the 15N (NO) NMR spectra ging N(2)–O(2) bond length of 1.224(4) Å (the bond angles
showing one broad signal (δ 58.3 ppm vs. MeNO2) in the NO Fe(1)–N(2)–O(2) 138.8(3)° and Fe(2)–N(2)–O(2) 131.0(3)°) is com-
region also support that complex 1 is fluxional, scrambling parable to the N–O bond distance of 1.26 Å in NO− and the
terminal and bridging NO ligands in d6-acetone at 320 K. N–O distance of 1.330(12) Å (the bent Fe–N–O) in [Fe(NO)4]−.8
Interestingly, complex 1 exhibits a diagnostic 15N (NO) NMR Of importance, the difference in bond distance between Fe(1)–
spectrum with bridging NO resonances (δ 200.8 and N(2) (1.761(3) Å) and Fe(2)–N(2) (1.967(3) Å) suggests that the
200.1 ppm vs. MeNO2) well-removed from the terminal NO reso- Fe(1) center in complex 1 would retain a {Fe(NO)2}9 core and
nances (δ 79.7, 73.5, 43.9, 30.3, 27.1 and 21.9 ppm) at 220 K Fe(2) permit a semibridging interaction of N(2)O(2) within the
(Fig. 1d). As elucidated by Mason and co-workers, the bent [(NO)Fe(μ-NO)Fe(NO)2] unit. This N(2)O(2) polarization may be
nitrosyl possessing a lower nN–π* excitation energy and a promoted by a semi-bridging electrostatic interaction with the
greater imbalance of charge in the valence shell giving a much immediate vicinity {Fe(NO)2}10 motif. This type of interaction
larger deshielding displays the downfield chemical shift (in may increase the nucleophilicity of semi-bridging NO, as is evi-
the range of 300–900 ppm) in the 15N NMR, compared to that denced by site-selective interaction of K+ at the bridging
of the linear nitrosyl (in the range of 20–200 ppm).6 The pres- nitroxyl oxygen (Fig. 2). The 150 cm−1 decrease in ν(NO) (RRS
ence of two sets of 15N (NO) NMR peaks (δ 200.8, 79.7, 43.9, vs. semi-bridging NO of complex 1) is believed to reflect the
21.9 ppm and δ 200.1, 73.5, 30.3, 27.1 ppm with a 3 : 1 ratio, strong electron donation from the electron-rich {Fe(NO)2}10
which are integrated on the basis of the similar environments motif to N(2)–O(2), thereby weakening both Fe(1)–N(2) and
of individual 15NO displaying similar relaxation mechanisms N(2)–O(2) bonds and lowering the corresponding stretching
in the ladder and boat forms) in complex 1 might be inter- frequency. Interestingly, the semi-bridging-NO stretching
preted either as equilibrium isotope effects or as two isomeric frequency (1510 cm−1 (KBr)) of complex 1 is comparable to
forms (ladder-form and, presumably, boat-form (inset of that of a semi-bridging interaction of NO within the [FeII–
Fig. 3)).6 The latter is preferred due to the significant differ- {Fe(NO)}7] unit, observed in Hr(NO) (mononitrosyl adduct of
ence in 15N chemical shift of the two species. It is noticed that the nonheme diiron protein hemerythrin) (1658 cm−1 (H2O))
the 15N NMR spectrum of complex 1 at 220 K displays δ 79.7, and FDP(NO) (1681 cm−1 (H2O)).4 In addition, the terminal
73.5, 43.9, 30.3, 27.1 and 21.9 ppm (terminal 15NO) in d6- N–O bond lengths (N(1)–O(1) 1.184(4), N(3)–O(3) 1.182(5) and
acetone falling within the range of δ −7.8 to 25.0 ppm and δ N(4)–O(4) 1.181(4)) of complex 1 are comparable to the range
23.1–76.1 ppm, the characteristic 15N NMR chemical shifts of [1.184(2)–1.187(3) Å] of the {Fe(NO)2}10–{Fe(NO)2}9 reduced-
{Fe(NO)2}10 and {Fe(NO)2}9 DNICs, respectively.7 Compared to form dinuclear DNICs.9 Therefore, the electronic structure
RRS displaying two absorption bands at 264 and 378 nm in of complex 1 may be best described as a coordinative assembly
the UV-vis spectrum,5b complex 1 shows absorption bands at of two fully delocalized [{Fe(NO)2}9–{Fe(NO)2}10] motifs. As is
273, 343 and 478 nm.
evidenced by the IR νNO spectrum (1510 cm−1), the bent Fe–
The single-crystal X-ray structure of the [Fe4(μ3-S)2- N–O bond angle (Fe(1)–N(2)–O(2) 138.8(3)° and Fe(2)–N(2)–
(μ2-NO)2(NO)6]2− unit in K+-18-crown-6-ether salt is depicted in O(2) 131.0(3)°) as well as the relatively long N–O bond distance
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(1.224(4) Å), the electronic structure of the bridging NO closely vibrations of two Fe2-semi-bridging NO motifs (Chart 1d),
approaches the nitroxyl anion (NO−).8
respectively. In boat-form B, the seven active NO vibrational
In order to gain more information about possible isomers frequencies were calculated to be 1726, 1682, 1678, 1667, 1645,
of complex 1, density functional theory (DFT) computations 1540 and 1538 cm−1. The detailed vibrational modes are de-
with the BP86 functional10 and a mixed basis set of SDD ECP11 lineated in ESI Chart S1.† As shown in Fig. 3, the combined
on Fe and 6-311++G(d,p)12 on all other atoms were employed calculated spectrum of forms A and B (3 : 1 ratio), displaying a
on ladder-form A and boat-form B (inset of Fig. 3).13 On the similar pattern to the experimental IR spectrum of complex 1
basis of the experimental and computational parameters sum- (ESI Fig. S1†), also supports two different isomers of complex 1
marized in Table S1,† the geometric parameters and nitroxyl with a 3 : 1 ratio in the 15N NMR at 220 K.
vibrational frequencies of ladder-form A are well comparable
The paramagnetic broadening of the 15N NMR peak of NO
to those of complex 1. The boat-form B is unstable compared groups at 300 K (or 250 K) (Fig. 1) suggests that the singlet-
to the ladder-form A by 1.7 kcal mol−1 (1.8 kcal mol−1) in the ground-state complex 1 has a low-lying triplet excited state
gas phase at 220 K (298 K). The 15NO-enriched boat-form with a small thermal population. In order to estimate the
B-15NO is found to be slightly unstable than the 15NO-enriched singlet/triplet energy splitting (ΔS/T), the magnetic suscepti-
ladder-form A-15NO by only 0.6 kcal mol−1 (0.7 kcal mol−1) in bility measurement of a powdered sample of complex 1 was
the solvation of acetone at 220 K (298 K), which corresponds to collected in the temperature range of 2–300 K at 0.5 T. The
an equilibrium constant KB/A ∼ 0.36 (0.31). Interestingly, this temperature-dependent effective magnetic moment decreases
value is consistent with the 3 : 1 ratio of two isomeric 1-15NO from 0.666μB at 300 K to 0.201μB at 2 K (ESI Fig. S2†). The best
observed in 15N NMR spectra (Fig. 1 and inset of Fig. 3). The fit to the data indicates that the low-lying triplet excited state is
calculated IR spectrum of conformation A displays four active higher than the singlet ground state by about 1843 2 cm−1
NO vibrational frequencies at 1696, 1682, 1645 and 1533 cm−1
,
with the g value for [{Fe(NO)2}9–{Fe(NO)2}10] fixed at 1.997
which mainly correspond to the anti-symmetric stretching (R2 = 0.991 and TIP = (141.6 3.3) × 10−6 cm3 mol−1) (ESI
vibrations of two central Fe-terminal NO motifs (Chart 1a), the Fig. S3†). Complex 1, measured in CH3CN with 0.1 M [nBu4N]-
two anti-symmetric stretching vibrations of two {Fe(NO)2} [PF6] as a supporting electrolyte at room temperature (scan
motifs (Chart 1b and c), and the anti-symmetric stretching rate 0.5 V s−1), displays a reversible redox wave at E1/2 = −1.72
V (vs. Cp2Fe/Cp2Fe+) with ΔEp = 150 mV and ipa/ipc = 0.92 (ESI
Fig. S4†). The redox potential of −1.72 V (vs. Cp2Fe/Cp2Fe+) for
complex 1 lies between that of RRS (−2.26 V vs. Cp2Fe/Cp2Fe+)
and that of RRE [(NO)4Fe2(μ-SEt)2] (−0.95 V vs. Cp2Fe/Cp2Fe+).5b
In contrast to the inertness of RRS toward HSCPh3, the
addition of 1 equiv. of [Cp2Fe][BF4] and HSCPh3 into a CH3CN
solution of complex
1
generates the known [{Fe(NO)}7–
({Fe(NO)2}9)3] [Fe4(μ3-S)3(NO)7]− (RBS) characterized by IR
(νNO) stretching frequencies shifting from (1742 w, 1701 s and
1668 m cm−1) to (1796 w, 1741 s, 1706 w cm−1), and nitric
oxide trapped by [PPN]2[S5Fe(μ-S)2FeS5] producing the known
complex [PPN][S5Fe(NO)2] (Scheme 1b).14 The conversion of
complex 1 into RBS triggered by one equiv. of S-donor species
HSCPh3 and oxidant [Cp2Fe][BF4] provided a facile pathway for
the transformation of RRS into RBS via complex 1.1b
Fig. 3 The calculated vibrational spectra for ladder-form A (blue line),
boat-form B (green line), and the combination of forms A and B (3 : 1
ratio) (red line).
In summary, the assembly of RRS and {Fe(NO)2}10 DNIC
[(TMEDA)Fe(NO)2] generating the iron–sulfur nitrosyl cluster 1,
a precursor of Roussin’s black salt (RBS), was discovered. Com-
pared to the {Fe(NO)2}9 and {Fe(NO)2}10 DNICs/RREs display-
ing 15N (NO) NMR chemical shifts (δ 23–76 ppm) and (δ −7.8
to 25 ppm),7 respectively, the first semibridging nitroxyl of
complex 1 exhibits the distinct 15N (NO) NMR chemical shift (δ
200.8 and 200.1 ppm vs. MeNO2). That is, the 15N (NO) NMR
chemical shift may serve as an efficient tool to discriminate
the binding forms of NO (terminal NO vs. semibridging NO
and straight M–NO vs. bent M–NO terminal links),6 in addition
to IR ν(NO) spectroscopy (e.g. observed in the diferrous site of
an FMN-free FDP (flavodiiron protein) triggering the turnover
of 2NO to N2O via a NO-semibridging FeII(μ-NO)FeIII inter-
mediate).4 In this study, we further showed how the electronic
structure of the coordinated NO groups of RRS is modulated
Chart 1 NO vibrational modes of ladder-form A.
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by the electronic richness of the immediate vicinity {Fe(NO)2}10
motifs.
We gratefully acknowledge financial support from the
National Science Council of Taiwan. We also thank Miss
Pei-Lin Chen and Mr Ting-Shen Kuo for single-crystal X-ray
structural determinations.
H.-W. Huang and W.-F. Liaw, Inorg. Chem., 2009, 48,
9027–9035; (c) P. P. Paul, Z. Tyeklár, A. Farooq, K. D. Karlin,
S. Liu and J. Zubieta, J. Am. Chem. Soc., 1990, 112,
2430–2432.
6 (a) J. Mason, D. M. P. Mingos, D. Sherman and
R. W. M. Wardle, J. Chem. Soc., Chem. Commun., 1984,
1223–1225; (b) J. Mason, L. F. Larkworthy and E. A. Moore,
Chem. Rev., 2002, 102, 913–934.
7 C.-C. Tsou, F.-T. Tsai, H.-Y. Chen, I.-J. Hsu and W.-F. Liaw,
Inorg. Chem., 2013, 52, 1631–1639.
Notes and references
8 Z.-S. Lin, T.-W. Chiou, K.-Y. Liu, C.-C. Hsieh, J.-S. K. Yu and
W.-F. Liaw, Inorg. Chem., 2012, 51, 10092–10094.
9 (a) C.-C. Tsou, T.-T. Lu and W.-F. Liaw, J. Am. Chem.
Soc., 2007, 129, 12626–12627; (b) T.-T. Lu, C.-C. Tsou,
H.-W. Huang, I.-J. Hsu, J.-M. Chen, T.-S. Kuo, Y. Wang and
W.-F. Liaw, Inorg. Chem., 2008, 47, 6040–6050.
1 (a) A. R. Butler and I. L. Megson, Chem. Rev., 2002, 102,
1155–1166; (b) K. Szaciłowski, A. Chmura and Z. Stasicka,
Coord. Chem. Rev., 2005, 249, 2408–2436.
2 (a) L. Calzolai, Z.-H. Zhou, M. W. W. Adams and G. N. Lamar,
J. Am. Chem. Soc., 1996, 118, 2513–2514; (b) D. H. Flint and
R. M. Allen, Chem. Rev., 1996, 96, 2315–2334.
10 (a) A. D. Becke, Phys. Rev. A, 1988, 38, 3098–3100;
(b) J. P. Perdew, Phys. Rev. B: Condens. Matter, 1986, 33,
8822–8824.
11 M. Kaupp, P. V. R. Schleyer, H. Stoll and H. Preuss, J. Chem.
Phys., 1991, 94, 1360–1366.
12 (a) R. Krishnan, J. S. Binkley, R. Seeger and J. A. Pople,
J. Chem. Phys., 1980, 72, 650–654; (b) A. J. H. Wachters,
J. Chem. Phys., 1970, 52, 1033–1036; (c) P. J. Hay, J. Chem.
Phys., 1977, 66, 4377–4384.
13 S. M. Brothers, M. Y. Darensbourg and M. B. Hall, Inorg.
Chem., 2011, 50, 8532–8540.
3 (a) C. E. Tinberg, Z. J. Tonzetich, H. Wang, L. H. Do,
Y. Yoda, S. P. Cramer and S. J. Lippard, J. Am. Chem. Soc.,
2010, 132, 18168–18176; (b) Z. J. Tonzetich, H. Wang,
D. Mitra, C. E. Tinberg, L. H. Do, F. E. Jenney Jr.,
M. W. W. Adams, S. P. Cramer and S. J. Lippard, J. Am.
Chem. Soc., 2010, 132, 6914–6916; (c) J. C. Crack, L. J. Smith,
M. R. Stapleton, J. Peck, N. J. Watmough, M. J. Buttner,
R. S. Buxton, J. G. Green, V. O. Oganesyan, A. J. Thomson
and N. E. Le Brun, J. Am. Chem. Soc., 2011, 133, 1112–1121.
4 T. Hayashi, J. D. Caranto, H. Matsumura, D. M. Kurtz Jr.
and P. Moënne-Loccoz, J. Am. Chem. Soc., 2012, 134,
6878–6884.
14 M.-L. Tsai, C.-C. Chen, I.-J. Hsu, S.-C. Ke, C.-H. Hsieh,
K.-A. Chiang, G.-H. Lee, Y. Wang and W.-F. Liaw, Inorg.
Chem., 2004, 43, 5159–5167.
5 (a) C.-C. Tsou, Z.-S. Lin, T.-T. Lu and W.-F. Liaw, J. Am.
Chem. Soc., 2008, 130, 17154–17160; (b) T.-T. Lu,
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