Hydrogen-Bonding Effects in Five-Coordinate High-Spin Imidazole-Ligated Iron(II) Porphyrinates

Article abstract of DOI:10.1021/acs.inorgchem.7b02744

The influence of hydrogen binding to the N-H group of coordinated imidazole in high-spin iron(II) porphyrinates has been studied. The preparation and characterization of new complexes based on [Fe(TPP)(2-MeHIm)] (TPP is the dianion of tetraphenylporphyrin) are reported. The hydrogen bond acceptors are ethanol, tetramethylene sulfoxide, and 2-methylimidazole. The last acceptor, 2-MeHIm, was found in a crystalline complex with two [Fe(TPP)(2-MeHIm)] sites, only one of which has the 2-methylimidazole hydrogen bond acceptor. This latter complex has been studied by temperature-dependent M?ssbauer spectroscopy. All new complexes have also been characterized by X-ray structure determinations. The Fe-N_P and Fe-N_Im bond lengths, and displacement of the Fe atom out of the porphyrin plane are similar to, but marginally different than, those in imidazole-ligated species with no hydrogen bond. All the structural and M?ssbauer properties suggest that these new hydrogen-bonded species have the same electronic configuration as imidazole-ligated species with no hydrogen bond. These new studies continue to show that the effects of hydrogen bonding in five-coordinate high-spin iron(II) systems are subtle and challenging to understand.

Full text of DOI:10.1021/acs.inorgchem.7b02744

Article
Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX
pubs.acs.org/IC
Hydrogen-Bonding Effects in Five-Coordinate High-Spin Imidazole-
Ligated Iron(II) Porphyrinates
Chuanjiang Hu,*
,†,‡
Bruce C. Noll,‡ Charles E. Schulz, and W. Robert Scheidt*
§
,‡
†Contribution from State and Local Joint Engineering Laboratory for Novel Functional Polymeric Materials, College of Chemistry,
Chemical Engineering and Materials Science, Soochow University, Suzhou 215123, Jiangsu, People’s Republic of China
‡
The Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, Indiana 46556, United States
§
Department of Physics, Knox College, Galesburg, Illinois 61401, United States
*
S Supporting Information
ABSTRACT: The influence of hydrogen binding to the N−H group of coordinated imidazole
in high-spin iron(II) porphyrinates has been studied. The preparation and characterization of
new complexes based on [Fe(TPP)(2-MeHIm)] (TPP is the dianion of tetraphenylporphyr-
in) are reported. The hydrogen bond acceptors are ethanol, tetramethylene sulfoxide, and 2-
methylimidazole. The last acceptor, 2-MeHIm, was found in a crystalline complex with two
[
Fe(TPP)(2-MeHIm)] sites, only one of which has the 2-methylimidazole hydrogen bond
acceptor. This latter complex has been studied by temperature-dependent Mossbauer
spectroscopy. All new complexes have also been characterized by X-ray structure
̈
determinations. The Fe−N and Fe−N bond lengths, and displacement of the Fe atom
P
Im
out of the porphyrin plane are similar to, but marginally different than, those in imidazole-
ligated species with no hydrogen bond. All the structural and Mossbauer properties suggest
̈
that these new hydrogen-bonded species have the same electronic configuration as imidazole-
ligated species with no hydrogen bond. These new studies continue to show that the effects of
hydrogen bonding in five-coordinate high-spin iron(II) systems are subtle and challenging to
understand.
INTRODUCTION
spectra are seen in both zero field and applied magnetic fields.
■
Spectra in applied magnetic fields show that the doubly
occupied d-orbital is different in imidazole- vs imidazolate-
ligated iron(II) porphyrinates. The positive sign of the
quadrupole splitting in the imidazolate derivative indicates
Understanding the importance of secondary coordination
sphere effects on the properties of biological coordination
complexes in proteins, including hemes, has attracted
considerable recent attention. Possible second coordination
sphere interactions include electrostatic interactions, π-
stacking, steric interactions, and hydrogen bonding. Of these,
1
,2
that the doubly occupied orbital must be the d -orbital,
xy
whereas the negative sign in the imidazole derivative is
consistent only with a low-symmetry orbital comprised of a
3
−7
hydrogen bonding effects are the most prevalent.
In heme
hybrid of d and an unoccupied porphyrin E(g) orbital. This
xz
proteins, the ligand binding pocket environment provides
hydrogen bonds to the coordinated axial ligand through the
protein side chains and can provide a wide range of hydrogen
change in the d-electron configuration is clearly consistent with
19,20
all observed differing features of the two classes.
hydrogen-bonded imidazoles fit into this divide?
Where do
8
−17
bond strengths thought to modulate protein function.
Directly studying how hydrogen bonding affects the
electronic structure and other properties of imidazole-ligated
high-spin iron(II) has proven to be quite challenging. The
requirements for adequate systems with imidazole-ligated N−
H hydrogen bonds are substantial. First, isolation of a well-
characterized solid-state material is a must. Obtaining five-
coordinate high-spin imidazole-ligated species requires steri-
cally hindered imidazoles (at the 2-position) to prevent
coordination of a second imidazole and thus stop formation
Heme proteins with histidine as the fifth ligand range from
(
a) the O -carrying/storing proteins with weak hydrogen
2
bonds from a nearby protein carbonyl to (b) peroxidases with
medium to strong hydrogen bonds to conserved aspartates to
c) oxidases with medium to strong hydrogen bonds to
(
conserved glutamates. Coordinated imidazolate has been taken
as the limit of a strong hydrogen bond. The differences
between coordinated imidazole and coordinated imidazolate
are quite profound but readily studied in small molecule
systems. Although imidazole- and imidazolate-ligated iron(II)
porphyrinates both exhibit an S = 2 (quintet) state, the
structural parameters of the coordination groups are distinct
with both axial and equatorial bond distance differences and
large differences in the displacement of iron from the
21
of a six-coordinate low-spin species. The imidazole must also
have an N−H group to interact with an added hydrogen-bond
acceptor. A possible complication is that the hydrogen bond
Received: October 26, 2017
1
8
porphyrin plane. Distinctive features in the Mossbauer
̈
©
XXXX American Chemical Society
A
DOI: 10.1021/acs.inorgchem.7b02744
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Inorganic Chemistry
Article
B
DOI: 10.1021/acs.inorgchem.7b02744
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Inorganic Chemistry
Article
MeHIm)·(C
spectroscopy, and the unit cell of the crystals used were checked
before the Mossbauer measurements. The crushed crystalline sample
H ssbauer
Cl), an 57Fe sample was prepared for Mo
̈
6 5
acceptor can lead to displacement of the original imidazole
ligand.
̈
An important result, which demonstrated how significant
hydrogen bonding can be, was found in an unusual crystalline
system that had two independent [Fe(TPP)(2-MeHIm)]
then was immobilized in Apiezon M grease mull.
Synthesis of 2[Fe(TPP)(2-MeHIm)]·(2-MeHIm)·(C H Cl). [Fe-
6
5
(
TPP)] O (32 mg, 0.024 mmol) was mixed with ethanethiol (1 mL)
2
2,23
2
molecules.
One molecule had an external 2-MeHIm as
in chlorobenzene (8 mL) and stirred for 3 days at room temperature.
The resulting solution of four-coordinate [Fe(TPP)] was transferred
into a Schlenk flask containing 2-methylimidazole (17 mg, 0.21
mmol) and 2,4,6-collidine (0.25 mL, 1.9 mmol). The mixture was
stirred for 1 h. X-ray-quality crystals were obtained in 8 mm × 250
mm sealed glass tubes by liquid diffusion using hexanes as nonsolvent
after five months.
the hydrogen bond acceptor; the other site had no hydrogen
bond to the coordinated imidazole. The system was
characterized by both X-ray and neutron diffraction structure
determinations and Mo
applied magnetic field. There were clear differences between
the sites. Both the structural details and the Mossbauer results
̈
ssbauer measurements in both zero and
̈
Synthesis of [Fe(TPP)(2-MeHIm)]·0.5(C H Cl). [Fe(TPP)] O
6
5
2
suggest that one site has imidazolate-like character and the
other site is comparable to other imidazole derivatives.
Attempts to replicate this strong hydrogen bonding via the
addition of several hindered pyridines as the hydrogen bond
acceptors either failed or, surprisingly, gave the same two-site
(
38 mg, 0.029 mmol) was mixed with ethanethiol (1 mL) in
chlorobenzene (8 mL), and stirred for 3 days at room temperature.
The resulting solution of four-coordinate [Fe(TPP)] was transferred
into a Schlenk flask containing 2-methylimidazole (75 mg, 0.93
mmol) and 2,4,6-collidine (0.25 mL, 1.9 mmol). The mixture was
stirred for 1 h. X-ray-quality crystals were obtained in 8 mm × 250
mm sealed glass tubes by liquid diffusion using hexanes as nonsolvent
after one month.
2
3,24
system.
A later attempt to study hydrogen-bonding effects made use
of 1,10-phenanthroline as the acceptor in five-coordinate high-
2
5
Synthesis of [Fe(TPP)(2-MeHIm)]·(C H OH). [Fe(TPP)] O (76
spin iron(II). This use of 1,10-phenanthroline followed
earlier results that demonstrated enhanced imidazole binding
2
5
2
mg, 0.058 mmol) was mixed with ethanethiol (1.5 mL) in
chlorobenzene (12 mL), and stirred for 3 days at room temperature.
The resulting solution of four-coordinate [Fe(TPP)] was transferred
into a Schlenk flask containing 2-methylimidazole (36 mg, 0.44
mmol). The mixture was stirred for 1 h. The resulting solution was
transferred into 8 mm × 250 mm sealed glass tubes and layered with a
2-methylimidazole solution (0.12 mol/L) in ethanol. X-ray-quality
crystals were obtained after 2 weeks.
26,27
contributions in six-coordinate iron(III) complexes.
The
consequences of the relatively weak hydrogen bonds formed
between coordinated imidazole and 1,10-phenanthroline were
found to have a small or no effect on the electronic structure of
the high-spin iron(II) species in either of the two species
characterized.
In this paper, we report on new attempts to obtain
crystalline materials with hydrogen bonding acceptors. This
investigation provides further examples with hydrogen-bonded,
coordinated imidazole with three examples described. All of
the new examples show that hydrogen bonding has only small
effects on either the electronic or molecular structures. Most
surprising was the isolation of a new two-site system with a
hydrogen-bonded imidazole site and a second site with no
hydrogen bond. Although there are many similarities between
Synthesis of [Fe(TPP)(2-MeHIm)]·TMSO. [Fe(TPP)] O (31
2
mg, 0.023 mmol) was mixed with ethanethiol (0.6 mL) in
chlorobenzene (6 mL), and stirred for 3 days at room temperature.
The resulting solution of four-coordinate [Fe(TPP)] was transferred
into a Schlenk flask containing 2-methylimidazole (11 mg, 0.13
mmol) and tetramethylene sulfoxide (TMSO, 0.5 mL, 5.8 mmol).
The mixture was stirred for 1 h. X-ray-quality crystals were obtained
in 8 mm × 250 mm sealed glass tubes by liquid diffusion using
hexanes as nonsolvent after 2 weeks.
X-ray Structure Determinations. Single-crystal experiments
were carried out on a Bruker Apex system with graphite-
monochromated Mo Kα radiation (λ = 0.71073 Å). All structures
23
this two-site system and an earlier system, the major effects
of hydrogen bonding observed in the first system are not
found. The new studies continue to show that the effects of
hydrogen bonding in five-coordinate high-spin iron(II)
systems are subtle and challenging to understand.
2
were solved by direct methods and refined against F using
32,33
SHELXTL;
subsequent difference Fourier syntheses led to the
location of most of the remaining non-hydrogen atoms. All
nonhydrogen atoms were refined anisotropically if not remarked
otherwise below. Hydrogen atoms were added with the standard
EXPERIMENTAL SECTION
34
■
SHELXL idealization methods. The program SADABS was applied
General Information. All reactions and manipulations for the
preparation of the iron(II) porphyrin derivatives (see below) were
carried out under argon, using a double-manifold vacuum line,
Schlenkware, and cannula techniques. Chlorobenzene was washed
with concentrated sulfuric acid, then with water until the aqueous
layer was neutral, dried with MgSO , and distilled twice over P O
for the absorption correction. Brief crystal data and intensity
collection parameters for the crystalline complexes are shown in
Table 1. Complete crystallographic details, atomic coordinates,
anisotropic thermal parameters, and fixed hydrogen atom coordinates
are given in the Supporting Information.
[Fe(TPP)(2-MeHIm)]·0.5(C H Cl). A red crystal with dimensions
4
2
5
6 5
under argon. Hexanes were distilled over sodium benzophenone. 2-
Methylimidazole (Aldrich) was recrystallized from toluene/methanol
and dried under vacuum. All other chemicals were used as received
from Aldrich or Fisher Scientific. The free-base porphyrin meso-
of 0.14 mm × 0.27 mm × 0.52 mm was used for the structure
determination. Crystal data were collected at 100 K. The structure
was refined in space group P2 /n with no restraints applied. The
1
asymmetric unit contains one porphyrinate molecule and half a
chlorobenzene solvate molecule. The 2-methylimidazole molecule was
found to be disordered over two positions. After the final refinement,
the occupancy of the major orientation was found to be 81%. The two
imidazole rings are essentially coplanar; the dihedral angle is ∼2.5°.
The chlorobenzene solvate is disordered around inversion centers.
[Fe(TPP)(2-MeHIm)]·(C H OH). A red crystal with the dimen-
tetraphenylporphyrin (H TPP) was prepared according to Adler et
2
28
al. The metalation of the free-base porphyrin to give [Fe(TPP)Cl]
was done as previously described. [Fe(TPP)] O was prepared
according to a modified Fleischer preparation. The Fe-enriched
porphyrinate was prepared using a modified small-scale metalation
29
2
3
0
57
3
1
57
procedure described by Landergren and Baltzer. The Fe O used
2
3
2 5
in the 57Fe labeled complex was purchased from Cambridge Isotopes.
Mossbauer measurements were performed on a constant
sions 0.43 mm × 0.08 mm × 0.07 mm was used for the structure
determination. Crystal data were collected at 100 K. The structure
was refined in space group C2/c with no restraints applied. The
molecule has required 2-fold symmetry and thus the asymmetric unit
contains a half porphyrinate molecule and a half ethanol solvate.
̈
acceleration spectrometer from 25 K to 250 K with optional small
field (Knox College) that was equipped with a Joule−Thompson
refrigerator for temperature control. For [Fe(TPP)(2-MeHIm)]·(2-
C
DOI: 10.1021/acs.inorgchem.7b02744
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Inorganic Chemistry
Article
Figure 1. ORTEP diagrams of three [Fe(TPP)(2-MeHIm)] molecules, all ellipsoids are contoured at the 50% probability level. For clarity, only
one orientation of the disordered imidazole ring and only the imidazole hydrogen N−H and methyl group hydrogen atoms are shown. The top
diagram is the [Fe(TPP)(2-MeHIm)]·0.5(C H Cl) solvate. The bottom left diagram is that for the [Fe(TPP)(2-MeHIm)]·(TMSO) solvate; the
6
5
N···O hydrogen bond distance is 2.744 Å. The bottom right diagram is that for the [Fe(TPP)(2-MeHIm)]·(EtOH) solvate; the N···O hydrogen
bond distance is 2.880 Å.
Figure 2. ORTEP diagram of the two [Fe(TPP)(2-MeHIm)] molecules in the two site system. Molecule 1′ is shown on the right (the coordinated
imidazole is disordered, with a major occupancy of 0.642). Molecule 2′ is shown on the left, with a completely ordered imidazole. The hydrogen
bond formed with the imidazole solvate has a N···N distance of 2.843 Å.
D
DOI: 10.1021/acs.inorgchem.7b02744
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Inorganic Chemistry
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[
Fe(TPP)(2-MeHIm)]·TMSO. A red crystal with the dimensions
DISCUSSION
■
0
.12 mm × 0.12 mm × 0.46 mm was used for the structure
We have been investigating the effects of deprotonation of
and/or hydrogen bonding to the N−H group of a coordinated
imidazole in five-coordinate high-spin iron(II) porphyrinates.
The effects of deprotonation of the imidazole are quite clear
and lead to substantial changes in both the coordination group
determination. Crystal data were collected at 100 K. The structure
was refined in space group C2/c. The molecule has required 2-fold
symmetry and, thus, the asymmetric unit contains half a porphyrinate
molecule and half a tetramethylene sulfoxide solvate molecule.
2
[Fe(TPP)(2-MeHIm)]·(2-MeHim)·(C H Cl). A red crystal with
6 5
1
8,35
the dimensions 0.29 mm × 0.31 mm × 0.32 mm was used for the
structure determination. Crystal data were collected at 100 K. The
geometry
and the electronic structure of the high-spin Fe
ssbauer
The sign of the quadrupole splitting of
center, including a change in sign of the Mo
̈
1
8,20,35
structure was refined in space group P1
The asymmetric unit contains two independent five-coordinate
Fe(TPP)(2-MeHIm)] molecules, one chlorobenzene molecule, and
one 2-methylimidazole molecule of solvation. The imidazole ligand
associated with molecule one is disordered with occupancies of 0.64
and 0.36. The two imidazole rings are essentially coplanar; the
dihedral angle is ∼2.2°. One phenyl ring of molecule one is
disordered with occupancies of 0.70 and 0.30. The chlorobenzene
solvate is also disordered with final refined occupancies of 0.75 and
̅
with no restraints applied.
splitting.
imidazole derivatives are negative, whereas that of imidazolate
derivatives are positive; this is the important consequence of
differing populations of the 3d electron manifold in these
[
6
high-spin complexes with a neutral vs an anionic axial
20,35
ligand.
The effects of hydrogen bonding to the imidazole are less
clear-cut. It might be expected that a strong hydrogen bond to
the imidazole would lead to imidazolate character for the
ligand and thus lead to changes for the overall complex as well.
This appeared to be the case in an earlier study, that of a two-
site system: one site with an imidazole solvate molecule
strongly hydrogen bonded to the imidazole of [Fe(TPP)(2-
MeHIm)] and the second site with no hydrogen bond.
Investigation showed that the first site had structural properties
tending toward that of imidazolate systems, whereas the
second site had geometric parameters typical of “normal”
imidazole derivatives. The Mossbauer spectra of this two-site
̈
system showed two distinct quadrupole doublets, with one
quadrupole doublet at least partially similar to the imidazolate
systems, although the sign of the quadrupole splittings could
0
.25. The second molecule is completely ordered.
RESULTS
■
The molecular structure of four iron(II) tetraphenylporphyri-
nates coordinated by the sterically hindered 2-methylimidazole
ligand are reported. The use of 2-methylimidazole ensures that
a high-spin five-coordinate complex results. Three crystalline
derivatives, illustrated in Figure 1, provide a structure for a
single [Fe(TPP)(2-MeHIm)] molecule. Two derivatives have
a hydrogen-bonded solvate molecule that are shown in the
diagrams. ORTEP diagrams with all atoms labeled are given in
the Supporting Information.
23
2
3
not be made with complete confidence. However, a later
study in which the coordinated imidazole was hydrogen-
bonded to the N atoms of 1,10-phenanthroline displayed much
smaller geometric effects and with the sign of the Mo
quadrupole splitting the same as that of imidazole systems with
Figure 2 displays the ORTEP diagram of an interesting
system containing two [Fe(TPP)(2-MeHIm)] molecules along
with a third 2-methylimidazole and a chlorobenzene molecule
as molecules of solvation in the asymmetric unit of structure.
ORTEP diagrams with all atoms labeled are given in the
Supporting Information. There are thought-provoking sim-
ilarities and differences with another system that has two
Fe(TPP)(2-MeHIm)] molecules along with a 2-methylimi-
dazole solvate in the asymmetric unit. These differences and
similarities will be discussed in detail in the Discussion section.
̈
ssbauer
2
5
no hydrogen bonding.
We hoped to clarify our understanding of these systems and
have now prepared additional five-coordinate high-spin
iron(II) species with a hydrogen-bonded imidazole. In this
paper, we report on four systems, three of which satisfy the
condition of an imidazole hydrogen-bonded to an external
acceptor. The results of these new studies show that the effects
of hydrogen bonding are subtle and challenging to understand.
All systems begin with the [Fe(TPP)(2-MeHIm)] base
complex. Two derivatives have either tetramethylene sulfoxide
[
23
Variable-temperature Mo
this two-site system. To ensure that the exact same phase as
the X-ray crystalline sample was measured by Mossbauer, an
̈
ssbauer spectra were obtained on
̈
5
7
Fe labeled sample was prepared and crystallized. Cell
or ethanol as the hydrogen bond acceptor. The ethanol
derivative has been reported previously,
constants were determined on several 5 Fe sample crystals.
These crystals were then crushed, immobilized, and measured.
Table 2 reports the measurements taken from 25 K to 298 K.
7
36,37
but complete
structural details were never published. The third derivative is a
two-site system with one [Fe(TPP)(2-MeHIm)] molecule
hydrogen-bonded to a 2-methylimidazole solvate molecule,
and the other [Fe(TPP)(2-MeHIm)] molecule is not
hydrogen-bonded. This system has some formal similarity to
a previously reported system, but significant differences are
found. The final derivative is a chlorobenzene solvate with no
hydrogen bond present.
We first consider structural aspects of these five-coordinate
high-spin iron(II) systems. The first structure of this type was
Fe(TPP)(2-MeHIm)]·(C H OH)
esting and unusual structural feature, that of a substantial
doming of the porphyrin core. This doming can be specified by
the difference in the displacement of the iron(II) from the
Table 2. Variable-Temperature Mo
[Fe(TPP)(2-MeHIm)]·(2-MeHIm)·(C H Cl)]
̈
ssbauer Parameters for
2
6
5
2
3
Line Width, Γ
mm/s)
(
temperature, T (K)
ΔEQ (mm/s)
δFe (mm/s)
left
right
2
2
2
1
1
95
50
00
50
00
1.818
1.873
1.985
2.053
2.171
2.254
2.266
0.796
0.832
0.862
0.876
0.887
0.897
0.900
0.276
0.307
0.325
0.341
0.328
0.322
0.210
0.273
0.303
0.322
0.327
0.316
0.323
0.205
3
6,37
[
that revealed an inter-
2
5
5
2
0
5
mean plane of the four N atoms (ΔN ) from the mean plane of
the 24-atom core (Δ). The Fe atom displacement values for
4
E
DOI: 10.1021/acs.inorgchem.7b02744
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Inorganic Chemistry
Article
a
Table 3. Selected Bond Distances and Angles for New Structures and Related Species
Bond Distances (Å)
Bond Angles (deg)
b
p
c
d
e
f
g
h
i
complex
Fe−N
Fe−Nim
ΔN4
Δ
Ct···N
Fe−N−C
Fe−N−C
θ
ϕ
ref
25
[
Fe(TPP)(2-MeHIm)]·
2.084(5)
2.1289(13)
0.38
0.47
2.049
132.03(12)
123.09(11)
8.8
18.5
(
1,10-phen) (A)
Fe(TPP)(2-MeHIm)]·
1,10-phen) (B)
[
2.080(9)
2.125(3)
0.36
0.39
2.049
130.8(2)
123.8(2)
6.6
17.7
25
(
2
.081(6)
2.120(3)
2.135(2)
0.36
0.39
0.38
0.49
2.051
2.051
133.7(2)
132.75(17)
121.5(2)
121.20(16)
5.4
2.7
7.8
8.1
25
25
[
Fe(OEP)(2-MeHIm)]·
1,10-phen)
2.088(14)
(
2
.087(14)
2.131(2)
2.161(5)
0.39
0.42
0.47
0.55
2.051
2.044
133.43(17)
131.4(4)
121.66(17)
122.6(4)
2.1
10.3
13.8
6.5
25
36
[
[
[
Fe(TPP)(2-MeHIm)]·
C H OH)
2.086(8)
2.087(12)
2.089(3)
(
2
5
Fe(TPP)(2-MeHIm)]·
C H OH)
2.144(1)
2.142(2)
2.136(13)
0.40
0.40
0.55
0.54
2.048
130.84(9)
131.48(13)
130.1(11)
123.32(9)
122.84
7.9
8.0
6.9
3.6
this
work
this
work
(
2
5
Fe(TPP)(2-MeHIm)]·
TMSO)
2.050
(
average of the eight values 2.084(4)
0.39(2)
0.48(7)
2.049(2)
122.5(9)
6.5(28)
10.(6)
[
[
[
[
[
Fe(OEP)(1,2-Me Im)]
Fe(OEP)(2-MeHIm)]
2.080(6)
2.077(7)
2.079(8)
2.076(3)
2.087(7)
2.171(3)
2.135(3)
2.158(2)
2.144(1)
2.155(2)
0.37
0.34
0.36
0.32
0.39
0.45
0.46
0.42
0.39
0.51
2.047
2.049
2.048
2.050
2.049
132.7(3)
131.3(3)
129.3(2)
132.8(1)
130.4(2)
121.4(2)
122.4(3)
124.9(2)
121.4(1)
123.4(2)
3.8
6.9
11.4
6.6
8.6
10.5
19.5
20.9
35.8
44.5
19
19
38
38
38
2
j
Fe(TPP)(1,2-Me Im)]
2
Fe(TTP)(2-MeHIm)]
j
Fe(Tp-OCH PP)(2-
3
MeHIm)]
[
[
[
Fe(Tp-OCH PP)(1,2-
2.077(6)
2.073(9)
2.084(11)
2.137(4)
0.35
0.38
2.046
131.9(3)
131.1(2)
130.67(9)
131.3(12)
122.7(3)
6.1
20.7
38
39
3
Me Im)]
2
j
Fe(TPP)(2-MeHIm)]·
2.127(3)
0.32
0.38
2.049
122.9(2)
8.3
24.0
1
.5(C H Cl)
6 5
j
Fe(TPP)(2-MeHIm)]·
.5(C H Cl)
2.1569(12)
2.148(15)
0.36
0.48
2.053
123.07(10)
122.8(11)
7.8
21.8
this
work
0
6
5
average of the eight values 2.079(5)
0.35(2)
0.43(5)
2.049(2)
7.4(22)
25.(10)
[
[
[
[
[
[
Fe(TPP)(2-MeHIm)]
2.080(8)
2.120(2)
2.099(2)
0.36
0.49
0.39
0.38
0.56
0.56
0.41
0.55
0.42
0.44
0.65
0.66
2.050
2.040
2.051
2.050
2.036
2.044
131.6(1)
129.0(1)
132.3(2)
132.0(2)
136.6(2)
129.6(3)
122.4(1)
125.7(1)
122.4(1)
122.9(2)
120.0(2)
126.7(3)
121.9(4)
9.2
7.6
7.9
4.1
3.6
9.8
16.0
22.9
12.4
40.5
37.4
23.4
23
23
(
Mol 1)
Fe(TPP)(2-MeHIm)]·(2- 2.099(7)
MeHIm) (Mol 2)
j
Fe(TPP)(2-MeHIm)]
Mol 1′)
2.084(9)
2.164(2)
this
work
this
work
(
Fe(TPP)(2-MeHIm)]·(2- 2.083(9)
2.125(2)
2.060(2)
1.999(5)
MeHIm) (Mol 2′)
K(222)][Fe(OEP)(2-
2.113(4)
18
−
MeIm )]
K(222)][Fe(TPP)(2-
2.118(13)
18
−
MeIm )]
2
.114(5)
133.6(4)
6.5
5.1
21.6
14.7
−
−
k
k
[
Fe(TpivPP)(2-MeIm )]
2.11(2)
2.002(15)
2.044(54)
0.52
0.55(2)
0.65
0.65(1)
2.045
2.042(5)
NR
NR
42
average of the three values 2.114(4)
a
b
c
d
Estimated standard deviations are given in parentheses. All complexes are high spin. Averaged value. Displacement of Fe from the mean plane
e
f
g
of the four pyrrole N atoms. Displacement of Fe from the 24-atom mean plane of the porphyrin core. 2-carbon, methyl-substituted. Imidazole 4-
carbon. Off-axis tilt (deg) of the Fe−N bond from the normal to the porphyrin plane. Dihedral angle between the plane defined by the closest
N −Fe−N and the imidazole plane in deg. Major imidazole orientation. Not reported.
h
i
Im
j
k
p
Im
this derivative were 0.42 and 0.55 Å or a doming of 0.13 Å.
Although this doming was initially thought to possibly be a
general stereochemical feature of high-spin five-coordinate
iron(II) derivatives, subsequent structure determinations of
several related species showed that there was a wide variety of
core conformations with an equally large variation in the (ΔN4
species pack isomorphously in similar crystallographic systems
(see Table 1). The values of the two displacements for all
hindered imidazole-ligated five-coordinate species are given in
Table 3, along with several additional structural parameters.
The first two groups given in Table 3 are derivatives with an
hydrogen-bonded imidazole and those without a hydrogen
bond acceptor. Both groups show wide variation in doming,
although the hydrogen-bonded group in the aggregate does
show slightly larger iron displacements from both types of
mean plane.
−
Δ) separation with values ranging from near zero to ∼0.15
1
9,25,38,39
Å.
Figures S5−S9 in the Supporting Information
display the pair of mean plane diagrams for each of the
derivatives in this study. The similar values for the hydrogen-
bonded ethanol solvate and the tetramethylene sulfoxide
solvate, both of which are at the upper limit of displacements,
may be the result of the crystal packing influences as these two
One possible effect of hydrogen bonding to the imidazole,
which, in the limit, can be thought of as an imidazolate, is
shown in Figure 3. The schematic on the left-hand side
F
DOI: 10.1021/acs.inorgchem.7b02744
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Figure 3. Schematic diagrams of the coordination group geometries found for a series of imidazole-ligated high-spin iron(II) porphyrinates with no
hydrogen bond (left), an analogous species with a strong hydrogen bond to the coordinated imidazole (center), and imidazolate-ligated high-spin
iron(II) porphyrinates (right). (Reprinted with permission from ref 25. Copyright 2008, American Chemical Society, Washington, DC.)
displays averaged values for several derivatives with no
hydrogen bonding, whereas the schematic on the right-hand
side shows averaged values from three derivatives, with
imidazolate as the axial ligand. The data for the middle
schematic comes from a single example with a hydrogen-
strong formal resemblance to an earlier study in which there
were also two such [Fe(TPP)(2-MeHIm)] sites, but the first
23
crystalline material did not have the chlorobenzene solvate.
The results of the distinct structures have been summarized in
the third group of derivatives displayed in Table 3. The two Fe
sites are labeled as Mol 1 and Mol 2, with the current results
also being denoted by prime symbols (Mol 1′ and Mol 2′).
Although the hydrogen bond between the solvate imidazole
and the coordinated imidazole are almost identical (the N···N
distances are 2.824 Å for the first species and 2.843 Å for the
new species), the coordination group geometries of Mol 2 and
Mol 2′ are very different. Mol 2 of the first system has
coordination group parameters that are much different from
either group 1 (hydrogen bonders) or group 2 (non-hydrogen
bonders) and much closer to that of imidazolate (the last
group of Table 3). However, the coordination group
parameters of Mol 2′ are similar to those of group 1. What
are the reasons for the large differences between the two
hydrogen-bonded species?
23
bonded imidazole that we will discuss later. Subsequent
studies with other hydrogen-bond acceptors to the imidazole
showed much smaller effects on the Fe atom displacements
and values of the Fe−N and Fe−N bond distances,
P
im
compared to the values displayed in the middle schematic of
Figure 3. Values for other stereochemical parameters are also
tabulated. There are an equal number of systems with no
hydrogen bonding to the coordinated imidazole that are given
in the second group of eight in Table 3. Averaged values for
the selected parameters for each class are also given in the
table. The estimated standard uncertainties following each
averaged value were calculated based on the assumption that
the values were drawn from the same population. The
differences in the averaged values of the hydrogen-bonded
derivatives, compared to those with no hydrogen bonds, are all
toward those of imidazolate derivatives, although the differ-
ences are marginally significant, if at all.
The additional solvate molecule (C H Cl) in the second
6
5
system will certainly change the packing in the two crystalline
solids. In principle, this allows a wide variety of differences in
molecular conformations. We note two possibly significant
differences, as a consequence of packing. The first is that there
is a second hydrogen bond in the original two-site crystal
system. The N−H group of the imidazole of Mol 1 forms a
hydrogen bond to a porphyrin nitrogen of Mol 2 with a
distance of 3.086 Å, thus leading to possible modest changes in
electron density at the Fe site in Mol 2. Generally,
intermolecular interactions in the second crystal system do
not appear substantially different, compared to the first system,
but there is no additional hydrogen bond in the first system.
The effect of this hydrogen bond must be to slightly increase
the electron density of iron, relative to when the second
hydrogen bond is not present.
Although the imidazole hydrogen atom was not located
experimentally in any of the reported derivatives, the idealized
position of the N−H hydrogen atom was used to calculate the
N−H···A angle. The values calculated were 166° for the EtOH
derivative, 170° for the TMSO derivative, and 166° for the
two-site system. A neutron diffraction study located the
hydrogen atom in the previous two-site system, where the N−
23
H···N angle was found to be 163(2)°.
The differences between most of the hydrogen-bonded
derivatives and the example shown in Figure 3 (center)
suggests the possibility that hydrogen bonding to coordinated
imidazole can lead to a rather large range of effects on the
coordination geometry and possibly on the electronic
structure. The final derivative of this study provides additional
evidence and understanding on this question. This final system
is 2[Fe(TPP)(2-MeHIm)]·(2-MeHIm)·(C H Cl). This crys-
A final important difference is found in the orientation of the
hydrogen-bonded imidazole, with respect to directions in the
40
porphyrin core. As has long been noted, the dihedral angle
6
5
talline species has two distinct [Fe(TPP)(2-MeHIm)] sites:
one with an imidazole solvate that hydrogen-bonds to the
coordinated imidazole and a second center with no hydrogen
bonding. This has been illustrated in Figure 2. There is a
between the imidazole plane and the closest Fe−N vector is
P
typically small, nearly eclipsing this closest Fe−N bond. The
P
observed values, usually called ϕ, are given for all imidazole
derivatives in Table 3. As a group, the averaged value of ϕ for
G
DOI: 10.1021/acs.inorgchem.7b02744
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
the hydrogen-bonded species is 10.4°; both the average value
and the range of values are smaller than those with no
hydrogen bond. The observed value of ϕ for Mol 2′ is clearly
much larger at 40.5°, outside the range of the commonly
observed values, and also much larger than that seen for Mol 2.
This suggests that a combination of imidazole orientation and
hydrogen-bonding influences are important in defining final
coordination group parameters. Unfortunately, our sample for
these possible effects is quite limited.
The steric bulk of the imidazole 2-methyl group leads to, in
all derivatives examined to date, an off-axis tilt of the axial Fe−
N
Im
bond and a rotation of the imidazole ligand that leads to
unequal Fe−N −C angles. The tilt angles range from 2.1°
Im
Im
for [Fe(OEP)(2-MeHIm)]·(1,10-phen) (Mol 2) to 11.4° for
Fe(TPP)(1,2-Me Im)]. This tilting is the partial result of
minimizing the interaction between the bulky imidazole methyl
group and the porphyrin core. Two important angles
Figure 4. Experimental Mo
̈
ssbauer spectrum of 2[Fe(TPP)(2-
[
2
MeHIm)]·(2-MeHIm)·(C H Cl) at 50 K. As described in the text,
6
5
the spectrum is believed to be a pair of quadrupole split doublets. The
diagram shows the fit made with the assumption that the areas and
line widths of the doublets are equal.
associated with the imidazole ligands (Fe−N −C ) are
Im
Im
given in Table 3. They range from 130.4(2)° to 133.7(2)° on
the methyl side and from 121.2(2)° to 123.8(2)° on the other
side. The off-axis tilt and imidazole rotation are correlated, to
maximize the distance between the 2-methyl group and
porphyrin core atoms; the values are similar across all
imidazole-ligated species.
ΔE decreases strongly with increasing temperature. A similar
Q
pattern has been observed for other five-coordinate high-spin
iron(II) porphyrinates with either tetraaryl or octaethyl
1
9,38
peripheral substituents
deoxyhemoglobin.
and for deoxymyoglobin and
4
1,49−54
The Mo
̈
ssbauer data for the two distinct two-iron site
The strong temperature dependence
systems clearly show that there are substantial differences
between Mol 2 and Mol 2′ and smaller differences between
Mol 1 and Mol 1′. Both Fe systems were measured on selected
of ΔE requires the presence of low-lying excited states above
Q
52,55
the quintet ground state.
What is the best description of the electronic structure for
imidazole-ligated high-spin iron(II) porphyrinates? Mossbauer
studies by Lang and co-workers first noted that the d-
single crystals labeled with 95% 57Fe to ensure Mo
ssbauer
̈
̈
41,49
sample integrity. The original two-site system displayed two
quadrupole doublets with distinct values of both the
quadrupole splitting and isomer shift. The present two-site
system shows an apparent single quadrupole doublet but with a
somewhat unusual temperature-dependent line widths. This
has been shown in Table 2. This is most consistent with a
electron manifold (of the quintet state) must be very
asymmetric, which requires that the d - and d -orbitals can
xz
yz
2
0
no longer be degenerate. DFT calculations, vetted by
agreement with other physical properties, including the sign
of ΔE , lead to the following description. The doubly occupied
Q
system displaying Mo
̈
ssbauer signals from two Fe centers with
d-orbitalthe d -orbitalis in a bonding combination with
xz
similar isomer shifts but with somewhat differing values of the
quadrupole splitting. An attempt to disentangle the two signals
using four overlapped Lorentzian lines, all with equal areas and
equal line widths, is shown in Table 4. An example spectral fit
one component of the unoccupied E
LUMO of the
g)
(
porphyrin ring. This orbital is located in the plane of the
coordinated imidazole. The next highest energy orbital is a
hybrid of the singly occupied d -orbital, in combination with
yz
the other component of the unoccupied E(g) LUMO of the
porphyrin ring. This electronic state is distinctly different from
that of high-spin derivatives with an anionic ligand where the
Table 4. Possible Partition of Mo
̈
2[Fe(TPP)(2-MeHIm)]·(2-MeHIm)·(C H Cl)]
doubly occupied orbital is the d -orbital. This leads to large
xy
temperature, T (K)
ΔE (mm/s)
Q
values of ΔE (and opposite sign) and slightly larger values
Q
2
2
2
1
95
50
00
50
1.934, 1.708
2.004, 1.742
2.118, 1.855
2.185, 1.920
2.391, 2.116
2.266
(
∼1.00 mm/s) for the isomer shift.
SUMMARY AND CONCLUSIONS
■
The synthesis and structures of four imidazole-ligated high-
spin iron(II) porphyrinates have been reported. These were
prepared as part of an effort to understand possible effects of
hydrogen bonding to coordinated imidazole. Three of the four
derivatives are found to have the desired hydrogen bond to
imidazole. An analysis of the structural parameters shows that
hydrogen bonding may have a small effect on geometry,
relative to derivatives with no hydrogen bond. This follows the
pattern now seen for hydrogen bonds versus no hydrogen
bond. The electronic structure of one derivative has been
5
2
0
5
at 50 K is shown in Figure 4. Although the two quadrupole
split doublets for 2[Fe(TPP)(2-MeHIm)]·(2-MeHIm)·
C H Cl)] do display differences, both the quadrupole
splitting values and the isomer shift values are clearly in the
range observed for imidazole-like species and not those of
imidazolate-like species, as can be seen from the tabulation and
(
6 5
comparisons given in Table 5. The Mo
two-site system also show that the effects of hydrogen bonding
are subtle and not easy to predict.
̈
ssbauer data for this
examined by temperature-dependent Mossbauer spectroscopy.
̈
This derivative has two Fe sites: one with hydrogen bonding to
the coordinated imidazole and one without hydrogen bonding
to the coordinated imidazole. Only small differences were seen
in the quadrupole splitting values, and no differences in the
Both Fe sites in this new two-site system show a strong
temperature dependence for the quadrupole splitting value.
H
DOI: 10.1021/acs.inorgchem.7b02744
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Table 5. Solid-State Mo
Related Species
̈
ssbauer Parameters for Five-Coordinate, High-Spin Imidazole-Ligated Iron(II) Porphyrinates and
a
b
complex
ΔEQ (mm/s)
−1.93
δFe (mm/s)
η
Γ
temperature, T (K)
ref
[
[
[
[
[
[
[
[
[
[
[
[
[
Fe(OEP)(2-MeHIm)]·(1,10-phen)
Fe(TPP)(2-MeHIm)]·(1,10-phen)
Fe(TPP)(2-MeHIm)·(C H OH))
0.94
0.90
0.93
0.92
0.90
0.95
0.94
0.92
0.85
0.86
0.92
0.92
0.88
0.92
0.92
0.90
0.90
0.92
0.97
1.00
1.00
0.97
1.03
1.05
1.03
1.06
0.84
0.83
0.83
1.01
0.76
0.43
0.30
0.31
0.37
0.41
0.46
0.58
0.44
0.42
0.43
0.50
0.25
0.40
0.30
0.34
4.2
20
25
25
41
19
19
38
38
38
38
38
39
41
43
41
41
c
−2.12
−2.28
−2.19
−1.94
−2.44
−2.18
−1.93
−1.95
−2.06
−2.40
−2.16
0.8
4.2
4.2
4.2
4.2
4.2
4.2
4.2
4.2
4.2
4.2
4.2
4.2
4.2
2
5
Fe(OEP)(1,2-Me Im)]
0.50
0.48
0.68
0.58
0.53
0.63
0.58
0.8
2
Fe(OEP)(2-MeHIm)]
Fe(Tp-OCH PP)(1,2-Me Im)]
3
2
Fe(Tp-OCH PP)(2-MeHIm)]
3
Fe(TPP)(1,2-Me Im)]
2
Fe(TTP)(2-MeHIm)]
Fe(TTP)(1,2-Me Im)]
2
Fe(TPP)(2-MeHIm)]
Fe(TPP)(1,2-Me Im)]
0.7
0.40
0.7
2
c
Fe((Piv C P)(1- MeIm)]
−2.3
2
8
deoxyHb
deoxyMb
−2.40
−2.22
> −2.27
< −2.27
−2.40
0.7
c
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
Fe(TPP)(2-MeHIm)] (Mol 1′)
Fe(TPP)(2-MeHIm)]·(2-MeHIm) (Mol 2′)
Fe(TPP)(2-MeHIm)] (Mol 1)
Fe(TPP)(2-MeHIm)]·(2-MeHIm) (Mol 2)
K(222)][Fe(OEP)(2-MeIm )]
this work
this work
23
c
d
0.90
0.71
0.22
0.02
0.37
0.58
0.31
0.32
4.2
4.2
4.2
4.2
77
4.2
4.2
4.2
4.2
4.2
4.2
4.2
77
d
+2.94
23
18
18
42
44
45
46
46
47
47
47
48
−
+3.71
+3.60
+3.51
−
K(222)][Fe(TPP)(2-MeIm )]
−
e
Fe(TPpivP)(2-MeIm)]
Fe(TPP)(OC H )]
−
+4.01
+4.25
+3.67
+3.90
+2.38
0.25
0.30
0.38
0.30
0.40
0.38
0.28
0.32
0.30
0.31
6
5
−
Fe)TPpivP)(O CCH )]
2
3
−
e
Fe(TPpivP)(OCH )]
3
−
e
Fe(TPpivP)(OC H )]
6
5
e
NaC H O ][Fe(TP P)(SC HF )]
12
24
6
piv
6
4
e
Na(222)][Fe(TpivPP)(SC HF )]
+2.38
6
4
−
Fe(TpivPP)(SC H )]
+2.18
+4.36
0.80
2
5
Fe(TpivPP)Cl]−
e
a
b
c
d
e
Asymmetry parameter. Line width, fwhm. Sign not determined experimentally, presumed negative. Sign is based on a best fit. Sign not
determined experimentally, presumed positive.
isomer shifts were observed between the two independent Fe
sites. None of the hydrogen-bonded systems of this study
displayed properties near those of imidazolate systems, unlike
emailing data_request@ccdc.cam.ac.uk, or by contacting The
Cambridge Crystallographic Data Centre, 12 Union Road,
Cambridge CB2 1EZ, UK; fax: +44 1223 336033.
23
the case in [Fe(TPP)(2-MeHIm)] ·2-MeHIm. We are left to
2
conclude that there is a gradation of effects from hydrogen
bonding, but with most displaying modest effects on geometry
and electronic structure, relative to systems with no hydrogen
bonding.
AUTHOR INFORMATION
■
Corresponding Authors
*
*
E-mail: scheidt.1@nd.edu (W.R.S.).
E-mail: cjhu@suda.edu.cn (C.H.).
ORCID
ASSOCIATED CONTENT
Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acs.inorg-
chem.7b02744.
■
Chuanjiang Hu: 0000-0001-7126-3789
Bruce C. Noll: 0000-0003-3962-4358
W. Robert Scheidt: 0000-0002-6643-2995
*
S
Notes
The authors declare no competing financial interest.
ORTEP and mean plane drawings (Figures S1−S9);
complete crystallographic details, coordinates, bond
distances and angles, and thermal parameters (Tables
S1−S24) (PDF)
ACKNOWLEDGMENTS
■
We thank the National Institutes of Health for support of this
research, under Grant No. GM-38401. We thank the NSF for
X-ray instrumentation support, through Grant No. CHE-
0443233.
Accession Codes
CCDC 1581485 (2[Fe(TPP)(2-MeHIm)]·(2-MeHim)·
(
1
(
C H Cl)), 1581486 ([Fe(TPP)(2-MeHIm)]·(TMSO)),
6 5
581487 ([Fe(TPP)(2-MeHIm)]·(C H OH)), 1581488 ([Fe-
REFERENCES
2
5
■
TPP)(2-MeHIm)]·0.5(C H Cl)) contain the supplementary
6 5
(1) Cook, S. A.; Borovik, A. S. Molecular Designs for Controlling the
Local Environments around Metal Ions. Acc. Chem. Res. 2015, 48,
2407−2414.
crystallographic data for this paper. These data can be obtained
free of charge via www.ccdc.cam.ac.uk/data_request/cif, or by
I
DOI: 10.1021/acs.inorgchem.7b02744
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
(
2) Lehnert, N. Elucidating second coordination sphere effects in
(23) Hu, C.; Noll, B. C.; Piccoli, P. M. B.; Schultz, A. J.; Schulz, C.
E.; Scheidt, W. R. Hydrogen Bonding Effects on the Electronic
Configuration of Five-Coordinate High-Spin Iron(II) Porphyrinates.
J. Am. Chem. Soc. 2008, 130, 3127−3136.
heme proteins using low-temperature magnetic circular dichroism
spectroscopy. J. Inorg. Biochem. 2012, 110, 83−93.
(
between oxidation state and hydrogen bond conformation in heme
proteins. Proc. Natl. Acad. Sci. U. S. A. 1979, 76, 1009−1013.
(
3) Valentine, J. S.; Sheridan, R. P.; Allen, L. C.; Kahn, P. Coupling
(24) Hu, C.; Scheidt, W. R. Unpublished observations.
(25) Hu, C.; Noll, B. C.; Schulz, C. E.; Scheidt, W. R. Hydrogen
Bonding Influence of 1,10-Phenanthroline on Five-Coordinate High-
Spin Imidazole-Ligated Iron(II) Porphyrinates. Inorg. Chem. 2008, 47,
8884−8895.
4) Quinn, R.; Mercer-Smith, J.; Burstyn, J. N.; Valentine, J. S.
Influence of hydrogen bonding on the properties of iron porphyrin
imidazole complexes. An internally hydrogen bonded imidazole
ligand. J. Am. Chem. Soc. 1984, 106, 4136−4144.
(26) Balch, A. L.; Watkins, J. J.; Doonan, D. J. Hydrogen bonding to
5) Zaric, S. D.; Popovic, D. M.; Knapp, E.-W. Factors Determining
́ ́
coordinated imidazole. Association of 1,10-phenanthroline and other
bases with bis(imidazole)metalloporphyrins. Inorg. Chem. 1979, 18,
(
the Orientation of Axially Coordinated Imidazoles in Heme Proteins.
Biochemistry 2001, 40, 7914−7928.
(
1
(
228−1231.
27) The increase in imidazole binding constants upon the addition
6) Sahoo, D.; Quesne, M. G.; de Visser, S. P.; Rath, S. P. Hydrogen-
of 1,10-phenanthroline had been noted previously by Abbott and
Rafson, but the origin of the effect has not been established. See:
Abbott, E. H.; Rafson, P. A. Enhancement of ligand binding by
iron(III) deuteroporphyrin(IX) dimethyl ester via interaction with
Bonding Interactions Trigger a Spin-Flip in Iron(III) Porphyrin
Complexes. Angew. Chem., Int. Ed. 2015, 54, 4796−4800.
(7) Salemme, F. R.; Freer, S. T.; Ng, H. X.; Alden, R. A.; Kraut, J.
The Structure of Oxidized Cytochrome c of Rhodospirillum rubrum. J.
2
1
,10-phenanthroline at a site remote from the metal ion. J. Am. Chem.
Soc. 1974, 96, 7378−7379.
28) Adler, A. D.; Longo, F. R.; Finarelli, J. D.; Goldmacher, J.;
Biol. Chem. 1973, 248, 3910−3921.
(8) Peisach, J.; Blumberg, W. E.; Adler, A. Electron Paramagnetic
(
Resonance Studies of Iron Porphyrin and Chlorin Systems. Ann. N. Y.
Acad. Sci. 1973, 206, 310−327.
Assour, J.; Korsakoff, L. A simplified synthesis for meso-
tetraphenylporphine. J. Org. Chem. 1967, 32, 476.
(9) Nicholls, P. The Role of The Protein In Haem Enzymes.
(29) (a) Adler, A. D.; Longo, F. R.; Kampas, F.; Kim, J. On the
Biochim. Biophys. Acta 1962, 60, 217−225.
10) Mincey, T.; Traylor, T. G. Anion Complexes of Ferrous
Porphyrins. J. Am. Chem. Soc. 1979, 101, 765−766.
11) Teraoka, J.; Kitagawa, T. Resonance raman study of the heme-
preparation of metalloporphyrins. J. Inorg. Nucl. Chem. 1970, 32,
(
2
443−2445. (b) Buchler, J. W. Static Coordination Chemistry of
Metalloporphyrins. In Porphyrins and Metalloporphyrins; Smith, K. M.,
(
Ed.; Elsevier Scientific Publishing: Amsterdam, The Netherlands,
linked ionization in reduced horseradish peroxidase. Biochem. Biophys.
Res. Commun. 1980, 93, 694−700.
1
(
975; Chapter 5.
30) (a) Fleischer, E. B.; Srivastava, T. S. The Structure and
(
12) Morrison, M.; Schonbaum, G. R. Peroxidase-Catalyzed
Properties of μ-Oxo-bis(tetraphenylporphineiron(III)). J. Am. Chem.
Soc. 1969, 91, 2403−2405. (b) Hoffman, A. B.; Collins, D. M.; Day,
V. W.; Fleischer, E. B.; Srivastava, T. S.; Hoard, J. L. The Crystal
Structure and Molecular Stereochemistry of μ-Oxo-bis[α,β,γ,δ-
tetraphenylporphinatoiron(III)]. J. Am. Chem. Soc. 1972, 94, 3620−
Halogenation. Annu. Rev. Biochem. 1976, 45, 861−888.
13) Peisach, J. An Interim Report on Electronic Control of
Oxygenation of Heme. Ann. N. Y. Acad. Sci. 1975, 244, 187−203.
14) Poulos, T. L. Heme Enzyme Structure and Function. Chem.
Rev. 2014, 114, 3919−3962.
15) Jensen, K. P.; Ryde, U. Importance of proximal hydrogen bonds
in haem proteins. Mol. Phys. 2003, 101, 2003−2018.
16) Berglund, G. I.; Carlsson, G. H.; Smith, A. T.; Szo
(
(
3
(
626.
31) Landergren, M.; Baltzer, L. Convenient small-scale method for
the insertion of iron into porphyrins. Inorg. Chem. 1990, 29, 556−557.
32) Sheldrick, G. M. A short history of SHELX. Acta Crystallogr.,
(
(
̈
ke, H.;
(
Henriksen, A.; Hajdu, J. The catalytic pathway of horseradish
Sect. A: Found. Crystallogr. 2008, A64, 112−122.
peroxidase at high resolution. Nature 2002, 417, 463−468.
2
2 2
(
33) R = ∑∥ F | − | F ∥/∑|F |, wR = {∑[w(F
− F ) ]/
1
o
c
o
2
o
c
(17) Gajhede, M.; Schuller, D. J.; Henriksen, A.; Smith, A. T.;
2
2
1/2
2
2
2
2
∑
[w(F ) ]} and R(F ) = ∑∥F | − |F | |/∑|F | . The conventional
R-factors R are based on F, with F set to zero for negative F . The
criterion of F > 2ρ(F ) was used only for calculating R . R-factors
o
o
c
o
Poulos, T. L. Crystal structure of horseradish peroxidase C at 2.15 Å
2
1
resolution. Nat. Struct. Biol. 1997, 4, 1032−1038.
2
2
1
(18) Hu, C.; Noll, B. C.; Schulz, C. E.; Scheidt, W. R. Proton-
2
based on F (wR ) are statistically about twice as large as those based
2
Mediated Electron Configuration Change in High-Spin Iron(II)
on F, and R-factors based on ALL data will be even larger.
Porphyrinates. J. Am. Chem. Soc. 2005, 127, 15018−15019.
(
34) Sheldrick, G. M. SADABS; Universitat
Germany, 2006.
35) Hu, C.; Schulz, C. E.; Scheidt, W. R. All High-Spin (S = 2)
Iron(II) Hemes are NOT Alike. Dalton Trans. 2015, 44, 18301−
8310.
36) (a) Collman, J. P.; Kim, N.; Hoard, J. L.; Lang, G.; Radonovich,
Gottingen: Gottingen,
̈ ̈ ̈
(19) Hu, C.; An, J.; Noll, B. C.; Schulz, C. E.; Scheidt, W. R.
Electronic Configuration of High-Spin Imidazole-Ligated Iron(II)
(
Octaethylporphyrinates. Inorg. Chem. 2006, 45, 4177−4185.
(20) Hu, C.; Sulok, C. D.; Paulat, F.; Lehnert, N.; Twigg, A. I.;
1
(
Hendrich, M. P.; Schulz, C. E.; Scheidt, W. R. Just a Proton:
Distinguishing the Two Electronic States of Five-Coordinate High-
Spin Iron(II) Porphyrinates with Imidazole/ate Coordination. J. Am.
Chem. Soc. 2010, 132, 3737−3750.
L. J.; Reed, C. A. Abstracts of Papers. In the 167th National Meeting of
the American Chemical Society, Los Angeles, CA, April 1974; American
Chemical Society: Washington, DC, 1974; Paper No. INOR 29.
(21) Collman, J. P.; Reed, C. A. Syntheses of Ferrous-Porphyrin
(37) Hoard, J. L. Personal communication to W.R.S. In particular,
Complexes. A Hypothetical Model for Deoxymyoglobin. J. Am. Chem.
Soc. 1973, 95, 2048−2049.
Prof. Hoard provided a complete set of atomic coordinates for the
molecule.
(22) The following abbreviations are used in this paper OEP,
(38) Hu, C.; Roth, A.; Ellison, M. K.; An, J.; Ellis, C. M.; Schulz, C.
dianion of octaethylporphyrin; TPP, dianion of meso-tetraphenylpor-
E.; Scheidt, W. R. Electronic Configuration Assignment and the
Importance of Low-Lying Excited States in High-Spin Imidazole-
Ligated Iron(II) Porphyrinates. J. Am. Chem. Soc. 2005, 127, 5675−
5688.
(39) Ellison, M. K.; Schulz, C. E.; Scheidt, W. R. Structure of the
Deoxymyoglobin Model [Fe(TPP)(2-MeHIm)] Reveals Unusual
Porphyrin Core Distortions. Inorg. Chem. 2002, 41, 2173−2181.
(40) Scheidt, W. R.; Chipman, D. M. Preferred Orientation of
Imidazole Ligands in Metalloporphyrins. J. Am. Chem. Soc. 1986, 108,
1163−1167.
phyrin; Tp-OCH PP, dianion of meso-tetra-p-methoxyphenylporphyr-
3
in; TTP, dianion of meso-tetratolylporphyrin, TpivPP, dianion of
α,α,α,α-tetrakis(o-pivalamidophenyl)porphyrin; Piv C P, dianion of
2
8
α,α,15-[2,2′-(octanediamido)diphenyl]-α,α,10−20-bis(o-pivalamido-
−
phenyl)porphyrin; 2-MeHIm, 2-methylimidazole; 2-MeIm , 2-meth-
ylimidazolate;1,2-Me Im, 1,2-dimethylimidazole; TMSO, tetramethy-
2
lene sulfoxide; 222, 4,7,13,16,21,24-hexaoxo-1,10-diazabicyclo[8.8.8]
hexacosane; N , porphyrinato nitrogen; Ct, the center of four
P
porphyrinato nitrogen atoms.
J
DOI: 10.1021/acs.inorgchem.7b02744
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
(
41) Kent, T. A.; Spartalian, K.; Lang, G.; Yonetani, T.; Reed, C. A.;
Collman, J. P. High Magnetic Field Mossbauer Studies of
Deoxymyoglobin, Deoxyhemoglobin, and Synthetic Analogues.
̈
Biochim. Biophys. Acta, Protein Struct. 1979, 580, 245−258.
(42) Mandon, D.; Ott-Woelfel, F.; Fischer, J.; Weiss, R.; Bill, E.;
Trautwein, A. X. Structure and spectroscopic properties of five-
coordinate (2-methylimidazolato)- and six-coordinate (imidazol-
(
2
imidazolato)iron(II) “picket-fence” porphyrins. Inorg. Chem. 1990,
9, 2442−2447.
43) Momenteau, M.; Scheidt, W. R.; Eigenbrot, C. W.; Reed, C. A.
(
A Deoxymyoglobin Model with a Sterically Unhindered Axial
Imidazole. J. Am. Chem. Soc. 1988, 110, 1207−1215.
(
44) Shaevitz, B. A.; Lang, G.; Reed, C. A. Susceptibility and
̈
ssbauer Analysis of a High-Spin Ferrous Synthetic Heme with
Mo
Unusually Large Quadrupole Splitting. Inorg. Chem. 1988, 27, 4607−
613.
45) Bominaar, E. L.; Ding, X.; Gismelseed, A.; Bill, E.; Winkler, H.;
Trautwein, A. X.; Nasri, H.; Fischer, J.; Weiss, R. Structural,
Mossbauer, and EPR Investigations on Two Oxidation States of a
4
(
̈
Five-Coordinate, High-Spin Synthetic Heme. Quantitative Interpre-
tation of Zero-Field Parameters and Large Quadrupole Splitting.
Inorg. Chem. 1992, 31, 1845−1854.
(46) Nasri, H.; Fischer, J.; Weiss, R.; Bill, E.; Trautwein, A. X.
Synthesis and Characterization of Five-Coordinate High-Spin Iron-
I1) Porphyrin Complexes with Unusually Large Quadrupole
(
Splittings. Models for the P460 Center of Hydroxylamine
Oxidoreductase from Nitrosomonas. J. Am. Chem. Soc. 1987, 109,
2
(
549−2550.
47) Schappacher, M.; Ricard, L.; Fischer, J.; Weiss, R.; Montiel-
Montoya, R.; Bill, E.; Trautwein, A. X. Synthesis, Structure, and
Spectroscopic Properties of Five-Coordinate Mercaptoiron(I1)
Porphyrins. Models for the Reduced State of Cytochrome P450.
Inorg. Chem. 1989, 28, 4639−4645.
(48) Schappacher, M.; Ricard, L.; Weiss, R.; Montiel-Montoya, R.;
Gonser, U.; Bill, E.; Trautwein, A. X. Synthesis and Spectroscopic
Properties of a Five-Coordinate Tetrafluorophenylthiolato Iron(II)
icket FencePorphyrin Complex and its Carbonyl and Dioxygen
Adducts: Synthetic Analogs for the Active Site of Cytochromes P450.
Inorg. Chim. Acta 1983, 78, L9−L12.
(
49) Kent, T. A.; Spartalian, K.; Lang, G. High magnetic field
Mossbauer studies of deoxymyoglobin, deoxyhemoglobin, and
synthetic analogues: Theoretical interpretations. J. Chem. Phys.
979, 71, 4899−4908.
50) Kent, T. A.; Spartalian, K.; Lang, G.; Yonetani, T. Mo
̈
1
(
̈
ssbauer
investigation of deoxymyoglobin in a high magnetic field. Orientation
of the electric field gradient and magnetic tensors. Biochim. Biophys.
Acta, Protein Struct. 1977, 490, 331−340.
(51) Eicher, H.; Bade, D.; Parak, F. Theoretical determination of the
electronic structure and the spatial arrangement of ferrous iron in
deoxygenated sperm whale myoglobin and human hemoglobin from
Mo
̈
ssbauer experiments. J. Chem. Phys. 1976, 64, 1446.
(52) Huynh, B. H.; Papaefthymiou, G. C.; Yen, C. S.; Groves, J. L.;
2
+
Wu, C. S. Electronic structure of Fe in normal human hemoglobin
and its isolated subunits. J. Chem. Phys. 1974, 61, 3750−3758.
(
53) Eicher, H.; Trautwein, A. Electronic Structure of Ferrous Iron
in Hemoglobin Inferred from Mo
Phys. 1970, 52, 932−934.
54) Eicher, H.; Trautwein, A. Electronic Structure and Quadrupole
Splittings of Ferrous Iron in Hemoglobin. J. Chem. Phys. 1969, 50,
540−2551.
55) Hori, H.; Yashiro, H.; Ninomiya, K.; Horitani, M.; Kida, T.;
Hagiwara, M. Low-lying electronic states of the ferrous high-spin (S =
) heme in deoxy-Mb and deoxy-Hb studied by highly-sensitive multi-
frequency EPR. J. Inorg. Biochem. 2011, 105, 1596−1602.
̈
ssbauer Measurements. J. Chem.
(
2
(
2
K
DOI: 10.1021/acs.inorgchem.7b02744
Inorg. Chem. XXXX, XXX, XXX−XXX