Study of an S = 1 NiII pincer electrocatalyst precursor for aqueous hydrogen production based on paramagnetic 1H NMR

Article abstract of DOI:10.1039/c3dt50528f

A tridentate NNN Ni^II complex, shown to be an electrocatalyst for aqueous H₂ production at low overpotentials, is studied by using temperature-dependent paramagnetic ¹H NMR. The NMR T₁ relaxation rates, temperat

Full text of DOI:10.1039/c3dt50528f

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PAPER
II
Study of an S = 1 Ni pincer electrocatalyst precursor
for aqueous hydrogen production based on
paramagnetic H NMR†
Cite this: DOI: 10.1039/c3dt50528f
1
a
a,b
a
c,d
Oana R. Luca, Steven J. Konezny,* Eric K. Paulson, Fatemah Habib,
a
c,d
a,b
a,b
Kurt M. Luthy, Muralee Murugesu, Robert H. Crabtree* and Victor S. Batista*
II
A tridentate NNN Ni complex, shown to be an electrocatalyst for aqueous H
2
production at low over-
relaxation rates,
1
potentials, is studied by using temperature-dependent paramagnetic H NMR. The NMR T
1
temperature dependence of the chemical shifts, and dc SQUID magnetic susceptibility are correlated to
DFT chemical shifts and compared with the properties of a diamagnetic Zn analogue complex. The result-
ing characterization provides an unambiguous assignment of the six proton environments in the meri-
dionally coordinating tridentate NNN ligand. The demonstrated NMR/DFT methodology should be
valuable in the search for appropriate ligands to optimize the reactivity of 3d metal complexes bound to
attract increasing attention in catalytic applications.
Received 27th February 2013,
Accepted 14th April 2013
DOI: 10.1039/c3dt50528f
www.rsc.org/dalton
Introduction
Understanding the nature of electrocatalytic pincer complexes
based on earth-abundant 3d transition metals is a subject of
great current interest due to the wide range of possible appli-
cations, including catalysis for hydrogen production and
1
,2
storage. Structure–activity relationships are fundamental to
catalyst optimization. However, characterization is often chal-
lenging due to the substitutional lability and paramagnetism
typical of 3d transition metal complexes. Therefore, there is an
urgent need to establish methodologies for this general class Fig. 1 Proton labeling for the NiNNN and ZnNNN complexes (left) and spin
populations of the NiNNN complex (right) calculated at the DFT UB3LYP/
of catalysts. NMR spectroscopy is a prime means of identifying
6-311++G(d,p) level of theory (excess α and β spin densities are shown on the
and characterizing diamagnetic precatalysts, and potential cata-
lytic intermediates. Extension to paramagnetic 3d metal com-
plexes remains underutilized because of the difficulties in
right in green (e.g., H ) and red (e.g., H ), respectively).
b
d
3
,4
signal assignment and interpretation of the NMR spectra.
to be an effective electrocatalyst for proton reduction under
1
Here, we apply paramagnetic H NMR spectroscopy in solution
to analyze a Ni NNN complex (Fig. 1) that was recently shown
2a
aqueous conditions. The diamagnetic reference shift, necess-
II
ary for the analysis, is obtained from the ZnNNN complex
specifically prepared for the NMR assignment.
When dissolved in DMSO, NiNNN has a diamagnetic NMR
spectrum, likely due to changes in coordination of the Ni
center. However, the NMR spectrum observed in non-coordi-
nating methylene chloride has broad line-shapes and unusual
chemical shifts, typical of paramagnetic complexes. Strong
magnetic interactions between the NMR active nuclei and
unpaired electrons typically lead to significant line broadening
and temperature-dependent chemical shifts that occur far
outside of the normal range of diamagnetic molecules,
making the usual methods of assigning and interpreting NMR
spectra inapplicable. In fact, routine structural assignments of
a
Department of Chemistry, Yale University, P.O. Box 208107, New Haven, CT 06520-
8
107, USA. E-mail: robert.crabtree@yale.edu, eric.paulson@yale.edu,
steven.konenzy@yale.edu, victor.batista@yale.edu
b
Energy Sciences Institute, Yale University, P.O. Box 27394, West Haven, CT 06516-
7
c
394, USA
Department of Chemistry, University of Ottawa, 10 Marie-Curie, Ottawa, Canada,
K1N 6N5
d
Centre for Catalysis Research and Innovation, University of Ottawa, 30 Marie Curie,
Ottawa, Canada, K1N 6N5
†
Electronic supplementary information (ESI) available. CCDC 926643. For ESI
and crystallographic data in CIF or other electronic format see DOI:
0.1039/c3dt50528f
1
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paramagnetic spectra generally remain inaccessible. While the between the nuclear magnetic moment and the magnetic
2
0
ratios of integrated peak areas can be helpful in making NMR moment of the unpaired electron treated as a point dipole.
assignments, in most paramagnetic cases including the Its contribution to the overall hyperfine shift δHF is most sig-
present study, line broadening induced by the paramagnetic nificant when the NMR active nucleus is in close proximity to
center leads to unreliable peak integration.
the paramagnetic center. Through-bond electron-nuclear inter-
Previous paramagnetic studies reported in the literature actions, due to electron spin delocalization onto nuclei that
often demonstrate the assignment of at most two or three interact with the resonating nucleus, determine the Fermi
4
21,22
proton environments. In the present work, we demonstrate contact shift:
the assignment and interpretation of the paramagnetic NMR
of NiNNN with six proton environments by combining DFT
2
2
μ0μB ge ðS þ 1Þ
δcon
¼
ρ
αꢀβ
ð3Þ
9
kBT
computations with NMR relaxation and variable temperature
5
measurements of chemical-shifts.
where μ is the vacuum permeability, μ is the Bohr magneton,
0
B
Paramagnetic NMR methods have been applied to elucidate ge is the free-electron g factor, S is the total spin of the system,
structural features in a variety of systems such as metallopro- kB is the Boltzmann constant, T is the absolute temperature in
6
7
teins, and metal complexes bound to DNA, including exper- K, and ρα−β is the residual spin density of the unpaired elec-
8
iments in the solid state. Our study of NiNNN complements tron on the nuclei that interacts with the resonating nucleus.
these earlier studies. Other paramagnetic 5-coordinate Ni com- While this treatment is strictly applicable for systems with neg-
9
,10
plexes with triplet ground states have been reported,
includ- ligible zero-field splitting (ZFS) and no deviations from Curie
5
ing the trigonal bipyramidal pyridine(2,6-diacetimidophenyl)- behavior (linearity of observed chemical shifts vs. 1/T), it pro-
dithiolate and diselenide complexes, a square pyramidal vides a useful approximation for systems with non-zero ZFS.
cysteine Ni complex, a complex of a penta-aza macrocyclic
ligand, nickel chelate thioether complexes and complexes affected by through-space dipolar interactions that accelerate
of tetradentate ligands with solvent coordination. Therefore, the relaxation times, typically determined via arrayed 1D NMR
we anticipate that the combined NMR/DFT methodology techniques. These longitudinal relaxation times T1N are
implemented in this study should be useful to address a approximately correlated to the distance r between the resonat-
variety of other paramagnetic 3d complexes such as five- ing nucleus and the paramagnetic center modeled as a point
1
1
23
1
2
The relaxation times of NMR-active nuclei are mostly
1
3
14
1
5
5
,16
coordinate nickel complexes
inspired by the active site of dipole, as follows:
[
Ni–Fe] hydrogenase as in the sulfate reducing bacterium
2
2
2
1
7
1
T1N
4SðS þ 1Þγ g β T
N
6
1e
Desulfovibrio gigas.
¼
ð4Þ
r
Here, T1e is the electron spin lattice relaxation time that is
often treated as a free parameter to be fitted to the observed
data since it can be difficult to determine at the temperatures
and magnetic fields used in NMR spectroscopy.
In our study of NiNNN, the dependence of the observed T1N
as a function of distance from the paramagnetic center was
1
Paramagnetic H NMR analysis
The theory of paramagnetic NMR spectroscopy is well estab-
5
,18
lished.
In paramagnetic molecules, interactions between
the nucleus and the unpaired electron spin(s) spread out the
observed chemical shifts δ over a much wider range than typi-
cally seen for diamagnetic molecules. The local electron cloud
around the resonating nucleus still provides an orbital contri-
bution δdia to the observed chemical shift, although the large
magnetic moment induced by the unpaired electron(s) pro-
vides a predominant additional contribution given by the
used to correlate and confirm the DFT-assisted assignment of
1
the paramagnetic NMR spectrum. Variable temperature
NMR data were collected in CD Cl
H
2
2
on a 500 MHz NMR instru-
ment in the temperature range from −80° to 20 °C. The direct
current (dc) magnetic susceptibility measurements were
carried out in the temperature range of 2.5–300 K under an
applied field of 1000 Oe.
1
9
temperature-dependent hyperfine shift δHF
:
δðTÞ ¼ δdia þ δHFðTÞ
ð1Þ
The orbital contribution is similar to the chemical-shift
observed for a diamagnetic analogue molecule (e.g., ZnNNN)
and is temperature independent to the extent that the molecu-
lar structure is temperature independent. In many cases, the
hyperfine shift δHF(T) can be accurately described as the sum
Results and discussion
Fig. 2 shows the dc magnetic susceptibility χT as a function of
temperature T in the 2.5–300 K range under an applied field of
3
1
000 Oe. The measured room temperature χT value is 1.34 cm
−
1
of the pseudocontact and Fermi shifts,
respectively:
con
δpc and δ ,
K mol , which is only slightly higher than the theoretical
3
−1
value of 1.00 cm K mol for a mononuclear Ni(II) complex
where g = 2.0. As the temperature decreases to 30 K, the χT
value slightly decreases before rapidly dropping to reach a
δHFðTÞ ¼ δpcðTÞ þ δconðTÞ
ð2Þ
3
−1
where δpc is determined by the electron-nuclear through-space minimum of 0.28 cm K mol at 2.5 K. This behavior is
interactions, typically modeled as the dipolar coupling indicative of depopulation of low-lying excited states and/or
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Fig. 2 Temperature dependence of the χT product for the NiNNN complex
under an applied dc field of 1000 Oe. Inset: Fitting of the 1/χ vs. T plot using
the Curie–Weiss law; the red line indicates the fit.
the presence of weak intermolecular antiferromagnetic inter-
actions between the mononuclear complexes. Fitting the 1/χ
vs. T plot (Fig. 2, inset) to the Curie–Weiss law yields a Curie
constant C = 1.42 and a Weiss constant θ = −6.14 K, confirm-
ing weak intermolecular antiferromagnetic interactions.
1
The magnetization plots, M vs. H and M vs. H/T, for NiNNN Fig. 3 (a) NiNNN variable temperature H NMR spectra collected in CD
2 2
Cl at
5
00 MHz and temperatures from −80° to 20 °C as indicated. Peaks labeled 1–6
from the most downfield to the most upfield in decreasing ppm values. (b)
(
presented in the ESI; Fig. S1-1 and S1-2†) show a field depen-
dence of the magnetization that does not saturate at low temp-
eratures (2.5 K) and high magnetic fields (up to 7 T) and
magnetization curves that are not superimposable on a single
master curve indicating the presence of magnetic anisotropy
and/or low lying excited states. The obtained data confirm the
paramagnetic nature of the five coordinate Ni(II) complex with
the expected S = 1 spin ground state.
1
Curie behavior of the H NMR chemical shifts shown in panel (a), including peak
1
b (black squares), 2e (red squares), 3d (blue circles), 4c (pink circles), 5a (green
triangles), 6f (purple triangles).
1
Fig. 3 shows the temperature-dependent H NMR data in
2 2
CD Cl , exhibiting six specific peaks with distinct T-dependent
chemical shifts as measured with a 500 MHz NMR instrument.
Fig. 3(b) shows that the chemical shifts change linearly as a
function of T− , consistent with Curie’s law, allowing for the
DFT assignment of the six proton environments, as described
below. DFT methods were used to correlate this linear behavior
with the calculated hyperfine term of the chemical shift
1
Fig. 4 Comparison of the X-ray structures of NiNNN (left) and ZnNNN (right)
complexes. ORTEP plots shown at 40% probability ellipsoids. H atoms are
δ
HF(T), as obtained according to the residual spin densities of omitted for clarity.
each proton and the orbital contribution estimated by the dia-
magnetic reference compound (ZnNNN), prepared specifically
for the purpose of providing a reliable temperature-indepen- complexes are sufficiently similar to have similar values of δdia
dent δdia
consistent with DFT calculations (Table 1).
The newly prepared diamagnetic ZnNNN complex has a tri-
Table 1 shows that the diamagnetic shielding constants cal-
,
.
gonal bipyramidal structure (Fig. 4, right), somewhat distorted culated at the DFT/UB3LYP/6-311++G(d,p) level of theory are in
due to the rigidity of the NNN ligand (.cif file in ESI†). In com- good agreement with the chemical shifts measured for the dia-
parison, the NiNNN complex (Fig. 4, left) has similar metal– magnetic reference (deviations between measured and calcu-
ligand distances and angles, although with a geometry closer lated data are less than 0.2 ppm). Having the orbital
to square pyramidal. Slight structural differences were also contribution, our preliminary assignments were made by cor-
observed in earlier comparisons of Zn and Ni analogs of relating the computed Fermi contact couplings with the exper-
5
b
4
-coordinate species. These results indicate that Zn and Ni imental values of δHF, determined by the slopes of the Curie
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1
26
Table 1 H NMR assignments for NiNNN, average distances r for isochronous protons obtained from the crystal structure of NiNNN, and calculated and experi-
mental values of the diamagnetic δdia and hyperfine δHF contributions to the chemical shifts. Experimental δdia corresponds to the chemical shift of the analogous
Zn compound. Calculated δHF assumes δHF ≈ δcon
NiNNN 10− T*δHF exp.
3
NiNNN 10−3T*δHF calc.
Proton
Peak
NiNNN r (Å)
ZnNNN δdia exp.
NiNNN δdia calc.
H
a
H
b
H
c
H
d
H
e
H
f
5
1
4
3
2
6
6.44
4.02
5.40
4.30
5.88
6.63
8.48
8.30
2.34
2.23
7.14
7.10
8.43
8.37
2.26
2.04
7.27
7.22
0.02 ± 0.08
6.18 ± 0.05
1.84 ± 0.07
2.10 ± 0.09
2.43 ± 0.06
−4.32 ± 0.09
−0.94
17.94
2.05
4.88
2.36
−4.72
plots (Fig. 3b) for protons far enough from the metal center for time leads to the assignment of H and H to peaks 1 and 3,
b
d
dipolar interactions to be small (δHF ≈ δcon). Comparison of respectively, since they correspond to the shortest measured T
experimental δHF and calculated δcon values in Table 1, with values.
1
particular attention to the sign of the slope and the metal–
proton distance, yields a direct assignment of peaks 2, 4, 5 and netic H NMR spectrum of NiNNN by combining temperature-
to protons H , H , H , and H , respectively. The remaining dependent NMR measurements and DFT methods. To the best
In summary, we have successfully assigned the paramag-
1
6
e
c
a
f
assignments can be made through the analysis of T values, as of our knowledge, this is the first time that paramagnetic NMR
1
described below.
of a compound with this level of complexity is fully assigned
Following the preliminary assignment based on calcu- and characterized. The methodology is simple and general, so
lations of δcon, we turned our attention to the pseudocontact it should be useful and applicable for a wide range of systems
interaction and its measurable effect on the nuclear longitudi- that permit analysis by paramagnetic NMR and DFT calcu-
nal relaxation T since the closer the proton is to the paramag- lations of chemical shifts. The analogous Zn compound pro-
1
net, the shorter the relaxation time should be. In order to vided the diamagnetic reference chemical shifts, essential for
obtain the through-space distances necessary for analysis, we the analysis. Assignment of all proton signals, including
averaged the distances between each isochronous proton in protons in proximity to the paramagnetic center, was possible
4
the crystal structure of NiNNN. The linear correlation between on the basis of temperature-dependent chemical shift
6
r and the measured relaxation time T
1
(Fig. 5) confirms the measurements, observations of T
1
relaxation times, and calcu-
existence of dipolar through-space interactions according to lations of diamagnetic shielding constants and isotropic Fermi
eqn (4). The data point corresponding to H is omitted from contact couplings. The analysis of the magnitude of observed
a
this analysis since the experimental peak is overlapped with relaxation times against distances in the crystal structure
other signals (making it difficult to obtain accurate inte- allowed a complete assignment of the six significantly broad-
1
II
grations) and T
1
is sensitive to slight changes in integration.
ened H NMR peaks of a redox-active NNN ligand in a Ni
2
a
The resulting correlation between the proximity of the complex.
proton to the paramagnetic center and the observed relaxation
Experimental
All reagents were received from commercial sources and used
without further purification unless otherwise specified. Sol-
vents were dried by passage through a column of activated
alumina followed by storage under dinitrogen. NMR spectra
were recorded on Bruker AMX 500 MHz spectrometers unless
otherwise specified. Chemical shifts are reported with respect
1
to a residual internal protio solvent for H. Literature pro-
2
4
cedures were utilized to synthesize NiNNN. Elemental ana-
lyses were performed by Robertson Microlit Inc.
2 2
NMR data were collected in CD Cl unless otherwise noted.
T
1
data were collected on a 500 MHz Bruker instrument at
−40 °C. The data were worked up using the Bruker Topspin T1/
T
2
relaxation module and MestReNova 5.2.4-3824. Exponential
fits and specific delays are available in the ESI.† (d1 = 2s, SW =
0, 64 scans per datapoint). Stacked spectra and delay details
5
are also available in the ESI.†
Variable temperature magnetic susceptibility measure-
ments were obtained using a Quantum Design SQUID
6
Fig. 5 Plot of r vs. T
1
relaxation for NiNNN. (source data available in S5†).
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MPMS-XL7 magnetometer which operates between 1.8 and
(b) O. R. Luca and R. H. Crabtree, Chem. Soc. Rev., 2013, 42,
1440–1459; (c) O. R. Luca, J. D. Blakemore, J. M. Praetorius,
T. J. Schmeier, G. B. Hunsinger, V. S. Batista,
G. W. Brudvig, N. Hazari and R. H. Crabtree, Inorg. Chem.,
2012, 51, 8704–8709.
3 (a) L. Sacconi, Pure Appl. Chem., 1968, 17, 95–127;
(b) I. Morassi, I. Bertini and L. Sacconi, Coord. Chem. Rev.,
1973, 11, 343–402; (c) L. Sacconi, G. P. Speroni and
R. Morassi, Inorg. Chem., 1968, 7, 1521–1525.
3
00 K for direct current (DC) applied fields up to 7 T.
Measurements were performed on a polycrystalline sample
of NiNNN (16.6 mg). The absence of ferromagnetic impurities
was confirmed by measuring the magnetization as a function
of field at 100 K. The magnetic data were corrected for the
sample holder and diamagnetic contributions from the
sample.
4
(a) T. O. Pennanen and J. Vaara, Phys. Rev. Lett., 2008, 100,
133002; (b) H. Liimatainen, T. O. Pennanen and J. Vaara,
Can. J. Chem., 2009, 87, 954; (c) J. Mao, Y. Zhang and
E. Oldfield, J. Am. Chem. Soc., 2002, 124, 13911;
Computational methods
Density functional theory calculations were performed using
2
5
Gaussian 09 and the B3LYP exchange–correlation functional
with unrestricted Kohn–Sham wave functions (UB3LYP). The
minimum energy structure of NiNNN (Fig. 1, right) was
obtained in the gas phase using a mixed basis with the
LANL2DZ basis set for Ni and the 6-311++G(d,p) basis set for
all other atoms. NMR shielding constants and Fermi-contact
terms were calculated using the gauge-independent atomic
orbital (GIAO) approach in conjunction with the polarizable
continuum model as implemented in Gaussian 09 with a
dielectric constant of ε = 8.93 (dichloromethane) for the conti-
(
d) R. Knorr, H. Hauer, A. Weiss, H. Polzer, F. Ruf, P. Löw,
P. Dvortsák and P. Böhrer, Inorg. Chem., 2007, 46, 8379;
e) P. Fernández, H. Pritzkow, J. Carbó, P. Hofmann and
(
M. Enders, Organometallics, 2007, 26, 4402; (f) M. Kruck,
D. C. Sauer, M. Enders, H. Wadepohl and L. H. Gade,
Dalton Trans., 2011, 40, 10406.
5
(a) L. Bertini and C. Luccinat, Coord. Chem. Rev., 1996, 150,
1
–296; (b) P. Roquette, A. Maronna, M. Reinmuth,
E. Kaifer, M. Enders and H.-J. Himmel, Inorg. Chem., 2011,
0, 1942–1955; (c) T. E. Manchonkin, M. W. Westler and
5
nuum solvating medium. Calculated values of δ
and
dia
J. L. Markley, Inorg. Chem., 2005, 44, 779–797.
I. Bertini, O. Turano and A. J. Vila, Chem. Rev., 1993, 93,
2
P. K. Bhattacharya, H. J. Lawson and J. K. Barton, Inorg.
Chem., 2003, 42, 8811–8817.
S. Ballayssac, I. Bertini, A. Bhaumik, M. Lelli and
C. Luchinat, Proc. Natl. Acad. Sci. U. S. A., 2008, 105, 17284–
−
3
1
0 T*δHF reported in Table 1 are an average of isochronous
6
7
8
protons, as defined in Fig. 1 (left). A reference chemical shift
of 31.77 ppm was used for the calculated values of δdia for
NiNNN (Table 1). This value was obtained by minimizing the
deviation from the values of δdia measured for the diamagnetic
reference (Table 1) and is in good agreement with a value of
833–2932.
3
1.97 ppm for tetramethylsilane calculated at the same level of
1
7289.
theory and solvent conditions.
9
E. W. Abel, R. J. Puddephatt, F. G. A. Stone and
G. Wilkinson, Comprehensive organometallic chemistry II:
a review of the literature, 1982–1994, Pergamon, 1995.
0 S. C. Davies, D. J. Evans, D. L. Hughes, S. Longhurst and
J. R. Sanders, Chem. Commun., 1999, 1935–1936.
1 C. A. Marganian, H. Vazir, N. Baidya, M. M. Olmstead and
P. K. Mascharak, J. Am. Chem. Soc., 1995, 117, 1584–1594.
2 S. A. Ross and C. J. Burrows, Inorg. Chem., 1998, 37, 5358–
Acknowledgements
1
1
1
1
1
1
The work was supported as part of the Center for Electrocataly-
sis, Transport Phenomena, and Materials (CETM) for Innova-
tive Energy Storage, an Energy Frontier Research Center
funded by the U.S. Department of Energy, Office of Science,
Office of Basic Energy Sciences under Award Number
DE-SC00001055. [OL, RHC for NMR experiments and assign-
ment; KL synthesis of ZNNN; EP help with data collection and
analysis; SJK, VSB computation component of assignment; FH,
MM Magnetism measurements]. We thank Prof. Jack Faller
and Prof. Gary Brudvig for useful discussions. We thank the
University of Ottawa, CCRI, NSERC (Discovery and RTI grants);
ERA, Vision 2010, CFI, ORF, FFCR. We thank Dr Nathan Schley
and Dr Michael Takase for the crystal structure refinement.
5
363.
3 E. Kimura and R. Machida, J. Chem. Soc., Chem. Commun.,
984, 499–500.
1
4 A. J. Blake, R. O. Gould, M. A. Halcrow and M. Schröder,
J. Chem. Soc., Dalton Trans., 1993, 2909–2920.
5 (a) H. Pannemann, S. Wassmann, J. Wilken, H. Gröger,
S. Wallbaum, M. Kossenjans, D. Hasse, W. Saak, S. Pohl
and J. Martens, J. Chem. Soc., Dalton Trans., 2000, 2467–
2
470; (b) M. Bröring, S. Prikhodovski and C. D. Brandt,
J. Chem. Soc., Dalton Trans., 2002, 4213–4218.
1
6 E. W. Abel, R. J. Puddephatt, F. G. A. Stone and
G. Wilkinson, Comprehensive organometallic chemistry II:
a review of the literature 1982–1994, Pergamon, 1995.
References
1
2
R. H. Crabtree, Energy Environ. Sci., 2008, 1, 134.
(a) O. R. Luca, S. J. Konezny, J. D. Blakemore, S. Saha,
17 M.-H. Volbeda, C. Charon, E. C. Piras, M. Hatchikian,
M. Frey and J. C. Fontecilla-Camps, Nature, 1995, 373, 580.
D. M. Colosi, G. W. Brudvig, V. S. Batista and 18 (a) NMR of Paramagnetic Molecules, ed. G. N. La Mar,
R. H. Crabtree, New J. Chem., 2012, 36, 1149–1152;
W. DeW. Horrocks Jr. and R. H. Holm, Academic Press,
This journal is © The Royal Society of Chemistry 2013
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View Article Online
Paper
Dalton Transactions
New York, 1973; (b) F. H. Köhler, Magnetism: Molecules to 21 R. S. Drago, Physical Methods for Chemists, Surfside Scienti-
Materials, ed. J. S. Miller, M. Drillon, Wiley-VCH, Wein- fic Publishers, 2nd edn, 1997.
heim, 2001, pp. 379–430; (c) I. Bertini, C. Luchinat and 22 L. Que Jr., Physical Methods in Bioinorganic Chemistry Spec-
G. Parigi, Prog. Nucl. Magn. Reson. Spectrosc., 2002, 40, 249; troscopy and Magnetism, University Science Books, 2000.
d) I. Bertini, C. Luchinat, G. Parigi and R. Pierattelli, Chem- 23 (a) M. J. Kurland and B. R. McGarvey, J. Magn. Reson., 1970,
(
BioChem, 2005, 6, 1536; (e) F. Rastrelli and A. Bagno,
Chem.–Eur. J., 2009, 15, 7990; (f) M. Kaupp and
F. H. Köhler, Coord. Chem. Rev., 2009, 253, 2376.
2, 286–381; (b) P. Rocquette, A. Maronna, A. Peters,
E. Kaifer, H.-J. Himmel, C. Hauf, V. Herz, E.-W. Scheidt
and W. Scherer, Chem.–Eur. J., 2010, 16, 1336–1350.
1
9 (a) I. Bertini, C. Luchinat and G. Parigi, Solution NMR of 24 H. Suzuki, S. Matsumura, Y. Satoh, K. Sogoh and
Paramagnetic Molecules- Applications to metallobiomolecules H. Yasuda, React. Funct. Polym., 2004, 77–91.
and Models, Elsevier, Amsterdam, 2001; (b) J. P. Jesson, 25 T. D. Manuel and J.-U. Rohde, J. Am. Chem. Soc., 2009, 131,
NMR of Paramagnetic Molecules- Principles and Applications,
Academic Press, New York, London, 1973.
0 Pseudocontact shift arises from the averaging of the δpc
due to tumbling in solution.
15582–15583.
26 M. J. Frisch, et al. GAUSSIAN 09 (Revision A.1), Gaussian,
Inc., Wallingford CT, 2009. See the ESI† for the complete
reference.
2
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