Article Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX
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How Does a Heme Carbene Differ from Diatomic Ligated (NO, CO, and CN−) Analogues in the Axial Bond? Qian Peng,‡ J. Timothy Sage,§ Yulong Liu,†,∥ Zijian Wang,‡,∥ Michael Y. Hu,⊥ Jiyong Zhao,⊥ E. Ercan Alp,⊥ W. Robert Scheidt,# and Jianfeng Li*,†
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College of Materials Science and Optoelectronic Technology, University of Chinese Academy of Sciences, Yanqi Lake, Huairou, Beijing 101408, China ‡ State Key Laboratory of Elemento-Organic Chemistry, College of Chemistry, Nankai University, Tianjin 300071, China § Department of Physics and Center for Interdisciplinary Research on Complex Systems, Northeastern University, Boston, Massachusetts 02115, United States ⊥ Advanced Photon Source, Argonne National Laboratory, Argonne, Illinois 60439, United States # Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, Indiana 46556, United States S Supporting Information *
ABSTRACT: Compared to well studied diatomic ligands (NO, CN−, CO), the axial bonds of carbene hemes is much less known although its significance in biological chemistry. The unusually large quadrupole splitting (ΔEQ = +2.2 mm· s−1) and asymmetric parameter (η = 0.9) of the fivecoordinate heme carbene [Fe(TTP)(CCl2)], which is the largest among all known low spin ferrohemes, has driven investigations by means of Mö ssbauer effect Nuclear Resonance Vibrational Spectroscopy (NRVS). Three distinct measurements on one single crystal (two in-plane and one out-of-plane) have demonstrated comprehensive vibrational structures including stretch (429) and bending modes (472 cm−1) of the axial Fe−CCl2, and revealed iron vibrational anisotropy in three orthogonal directions for the first time. Frontier orbital analysis especially comparisons with diatomic analogues (NO, CN−, CO) suggest that CCl2, similar to NO, has led to strong but anisotropic π bonding in a ligand-based “4C”-coordinate which induced the vibrational anisotropies and very large Mössbauer parameters. This is contrasted to CN− and CO complexes which possess a porphyrin-based “4N”-coordinate electronic and vibrational structures due to inherent onaxis linear ligation.
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axial bonds as active sites.9,10 However, the knowledge of the axial bonds which are essential to understand the reaction mechanism is rather scarce, for example, debates remain on the iron oxidation and electronic configurations of the Fe−Ccarbene bond (FeII−(CR)0 ↔ FeIII−(CR)−1).11,12 Recently, we have reported studies on several five-coordinate iron porphyrin carbene complexes which definitely assigned low spin state (S = 0) of the iron(II) centers.13 Surprisingly, the (high field) Mössbauer characterizations have suggested unusually large quadrupole splitting ΔEQ = +2.2 mm·s−1 and asymmetric parameter of the electric field gradient η = 0.9 for [Fe(TTP)(CCl2)],14 which are the largest among all the known low spin ferrohemes (vs |ΔEQ| < 1.8 mm·s−1 for CN− and CO analogues).13 The only complex which show comparable values are the oxyhemes where two analogous electronic configurations of FeII−(O2)0 ↔ FeIII−(O2)−1 have
INTRODUCTION The axial bonds of hemes are the active sites where many biochemical processes happen, thus, its properties dramatically affect the functions of enzymes.1,2 For the diatomic ligands, such as NO, CO, and CN−, which serve as signal molecules, regulators, and/or inhibitors, the formation of axial bonds might change iron oxidation states,3 spin states, and the strength of the proximal bonds, for example, the strong trans effects of NO has long been recognized,4 Numerous efforts have been directed to these heme complexes and considerable progresses have been gained about the Fe−XY bonds including the geometric, electronic, and vibrational information.2,5,6 In contrast, the axial bonds of some heme complexes actively involved with the biosynthesis of various substrates. For example, the iron-carbene and -oxo hemes, both of which are regarded as intermediates of cytochrome P450 enzymes,7,8 have drawn much research attentions for their excellent catalytic performance in various carbon (e.g., C−H insertion) and oxygen (e.g., epoxidation) atom transfer reactions with the © XXXX American Chemical Society
Received: March 5, 2018
A
DOI: 10.1021/acs.inorgchem.8b00574 Inorg. Chem. XXXX, XXX, XXX−XXX
Article
Inorganic Chemistry also been disputed for many years.15−17 Hence, reasonable interpretations on the large ΔEQ and η appear required to thoroughly clarify the Fe−Ccarbene bond. Given asymmetric parameter η = (Vxx − Vyy)/Vzz, with the maximum being 1, the value of 0.9 must indicate a very strong anisotropy in the porphyrin plane. A method that could directly afford quantitative information for distinct molecular orientations appears promising to study such an object. NRVS, a synchrotron based technology that provides vibrational and electronic structures of Mössbauer-active complexes, has recently emerged as a powerful method.18−20 In particular, the single crystal NRVS which is unique to probe the vibrational anisotropy of iron and gives insights into the (axial) bond nature has been practically developed and suitable to current study.21,22
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The frontier orbital interactions between the occupied iron d orbital and CCl2 carbene π* empty orbital has been illustrated as the molecular bonding orbital HOMO−3 and antibonding orbital LUMO +2 in Figures S9 and S10. For [Fe(TPP)(CN)]−, there is a small electronic energy difference (2.5 kcal/mol) between high spin (S = 2) and low spin (S = 0) states. Electronic Structure and NRVS Calculations. The G09 program package29 was used to optimize the structures and for frequency analysis in our study. The model complex [Fe(TTP)(CCl2)], [Fe(TPP)(CN)]− and [Fe(TPP)(CO)] were fully optimized without any constraints by using the Hybrid-GGA functional B3LYP30−33 with Grimme’s D3 dispersion correction.34 The triple-ζ valence basis sets def2-TZVP35 was used for Fe, and 6-31+G* basis sets for axial ligand (CCl2, CN−, and CO) and nitrogen atoms on porphyrin, 6-31G* basis set for all other atoms. Two different spin states low-spin (S = 0) or high spin (S = 2) of model complex were calculated in order to estimate ground states. Free energies were evaluated at 298.15 K and 1 atm using harmonic vibrational frequencies at the same basis level. The frequency output data have been printed using the high precision format vibrational frequency eigenvectors to calculate Mode Composition Factors (e2) and Vibrational Density of States (VDOS). The mode composition factors e2jα, which represent the fraction of the kinetic energy in frequency mode due to the motion of atom j (j = 57 Fe for NRVS), and provide a convenient quantitative comparison between measurements and calculations. Mode composition factors are defined in eq 1:
EXPERIMENTAL SECTION
All reactions and manipulations were carried out under argon using a double-manifold vacuum line, Schlenkware, and cannula techniques unless otherwise specified. Benzene and THF were distilled over sodium/benzophenone and dichloromethane over CaH2. Hexanes was distilled from sodium/potassium alloy and chlorobenzene (Sinopharm Chemical Reagent) over P2O5 under nitrogen. Methanol was distilled from CaH2 and refluxed over magnesium. CCl4 (aladdin chemicals) was purified according to standard methods.23 KH (aladdin chemicals) was stored in the drybox and washed with hexanes before use. [H2(TTP)] were prepared according to Adler et al.24 Single Crystal [57Fe(TTP)(CCl2)]. The reaction procedures described previously were used for the sample preparation.13 A dark-purple block-shaped crystal with the dimensions of 0.40 × 0.40 × 0.79 mm3 was used for the structure determination and NRVS experiments (a, 12.6869(10); b, 13.4548(10); c, 14.0726(10) Å; α, 74.813(2); β, 78.417(2); γ, 81.985(2)°; v, 2261.5(3)). NRVS Crystal Mounting. A detailed crystal alignment and NRVS measurement program has been developed.25 Crystals were mounted onto specially prepared dual arc goniometer heads. Copper wire, 4−5 cm in length and 18 gauge, was affixed to the goniometer and bent into a u-shape. A glass fiber, 5−8 mm in length, was then superglued to project along the goniometer ϕ-axis. The connection of the wire into the goniometer head was fortified with epoxy resin. A crystal was then affixed to the tip of the glass fiber using super glue. The wire was then carefully bent so that the crystal was approximately on the ϕ-axis and then stretched to the required height for centering. Crystals were then oriented for NRVS analysis along specified in-plane axes by methods described.25 NRVS Spectra. Spectra were measured at Sector 3-ID of the Advanced Photon Source, Argonne National Laboratory, Argonne, IL. Single-crystal samples were previously mounted and aligned on goniometer heads that were screwed into place on a rotating stage. The mounted crystals were then located into the X-ray beam by translations of the stage and rotated to the predetermined ϕ-angle required for the particular direction of analysis desired. A stream of cold N2 gas from a commercial cryocooler controlled crystal temperature during NRVS measurements. Typical temperatures at the crystal is 100 K. Vibrational spectra were measured using an inline high-resolution monochromator operating at 14.4125 keV with 1.0 meV bandwidth scanning the energy of incident X-ray beam.26 Spectra were recorded between −30 and 80 meV in steps of 0.25 meV, and all scans (3−6 replicates) were normalized to the intensity of the incident beam and added. NRVS raw data were converted to the vibrational density of states (VDOS) using the program PHOENIX.27,28 NRVS measurements were made in three orthogonal directions for [57Fe(TTP)(CCl2)]. DFT Calculations. DFT calculations on [Fe(TTP)(CCl2)] at B3LYP-D3 level of theory predicted low spin (S = 0) is 11.1 kcal/mol more stable than high spin (S = 2) in electronic energy, which indicate only low spin complex can be observed in the experiment.
ej2α =
mjr j2 ∑ miri2
(1)
where the mi is the atomic mass of atom i and ri is the absolute length of the Cartesian displacement vector for atom i in Angstroms. The Mode Composition Factors for different directions are defined in terms of an averaged porphyrin plane as in-plane, which can be calculated from a projection of the atomic displacement vector x and y (eq 2). The out-of-plane atomic displacement perpendicular to the resulting porphyrin plane for a normal mode is obtained from a projection of the atomic displacement vector z (eq 3). ej2α ,in‐plane =
mj(r jx2 + r jy2 )
ej2α ,out‐of‐plane =
∑ miri2
(2)
mjr jz2 ∑ miri2
(3)
The scripts can be used to calculate the mode composition factors with designated direction.35 In this paper, the X direction (green color) and Y direction (red color) were parallel and perpendicular to the plane of axial ligand Cl−C−Cl. Vibrational Density of States (VDOS) intensities can be simulated from the Mode Composition Factors using the Gaussian normal distributions function through MATLAB.
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RESULTS AND DISCUSSION NRVS spectra were collected on one 57Fe enriched single crystal of [Fe(TTP)(CCl2)] (P-1) in one out-of-plane and two in-plane orientations. DFT calculations at the B3LYP-D3 level, which have suggested a stable singlet state (11.1 kcal/mol below the quintet), are applied to predict the vibrational dynamics. The measured and DFT predicted out-of-plane spectra are given in Figure 1. It is seen both spectra show five resolved peaks which are consistent to each other. The most intense peak is found at 429 cm−1 which was expected to be the Fe−Ccarbene stretch mode. NRVS studies on the fivecoordinate heme complexes with diatomic ligands (NO, CO and CN−) have revealed a linear relationship between the axial distances and Fe−Laxial stretch modes with shorter bond B
DOI: 10.1021/acs.inorgchem.8b00574 Inorg. Chem. XXXX, XXX, XXX−XXX
Article
Inorganic Chemistry
and two chlorine atoms are along the bonds and toward the carbon atom, thus in the same ligand plane. In contrast, the carbon atom appears static and locates in the center of the plane. Therefore, the vibration at 429 cm−1 is a mixed mode consisting of Fe−C and C−Cl stretches, rather different from the other vibrations of Figure 2. Such mixing of vibrational modes can interfere with the correlation of corresponding vibrational frequencies with other properties of the complex. One way to deal with this is to consider force constants. Previously Lehnert and co-workers have reported modes analysis of ferrous and ferric nitrosyl porphyrinates by correlating the metal−ligand force constants with the metal− ligand distances.36,37 The second peak at 309 is predicted at 316 cm−1. The character of this mode is illustrated in Figure S1, which suggests a typical r6 vibration.35,36 The Fe−C bond and the porphyrin core atoms (except the Cβ atoms) vibrate toward each other, both of which are perpendicular to the porphyrin plane. The carbene ligand shows strong Cl−C−Cl bending character, which is also found in the third resolved peak at 256 cm−1. In this mode (249 cm−1, Figure S2), the Fe−C bond moves towards the porphyrin core with the iron showing very strong motion. In the porphyrin core, one pair of pyrrole rings show typical Fe−Np stretches, while the other pair shows motions similar to those of the pyrroles in the doming mode r9, which is observed at 117 cm−1 (99 cm−1, Figure S3).38,39 In the NRVS study of nitrosyl [Fe(OEP)(NO)], Pavlik et al. reported the axial ligand based vibrational anisotropy and suggested the anisotropy reflected asymmetric interactions between Fe dπ and NO π* orbitals parallel and perpendicular to the FeNO plane.25,40 Later analogues with axial ligand of imidazole41,42 or imidazolate43 were also investigated. However, neither case represented anisotropic behaviors such as that of [Fe(OEP)(NO)]. Interestingly, [Fe(TTP)(CCl2)] demonstrated very pure vibrational anisotropy in all three orthogonal directions. A stacked bar graph, which illustrates the predicted x, y, and z components of the iron kinetic energy fractions, is given in Figure 4. As can be seen, all the modes (with e2Fe > 0.025) have iron motion solely along one of the three distinct directions. This contrasts with [Fe(OEP)(NO)], where the z directional modes are mixed with x and y vibrations.25,40
Figure 1. Measured (blue) and DFT predicted (black) VDOS (vibrational densities of states) of [Fe(TTP)(CCl2)] along the direction of out-of-plane.
distances corresponding to stronger stretches.18 A plot with the addition of current parameters is given in Figure 2. As can be
Figure 2. Plot showing the correlation of the Fe−L stretching frequencies determined by NRVS with the observed (X-ray) Fe−L bond lengths for the five-coordinate derivatives. The red line is fitted for diatomic ligands.
seen, although CCl2 shows a similar axial distance (1.7295(15) Å) to the others, its frequency appears at a much lower position, suggesting its character may be substantially different from the others. The predicted vibration (444 cm−1) is illustrated in Figure 3. It is seen the strong motion of the iron
Figure 4. Complete predicted spectrum of [Fe(TTP)(CCl2)] further showing the directional components in three orthogonal directions (as eFe2 values, bars).
Figure 3. Predicted modes at 444 cm−1. C
DOI: 10.1021/acs.inorgchem.8b00574 Inorg. Chem. XXXX, XXX, XXX−XXX
Article
Inorganic Chemistry
character is given in the left panel of Figure 6. As can be seen, the modes at 471 and 512 cm−1 shared common features. Both iron motions are along the Cmeso atoms, while perpendicular to each other, as observed in x or y direction. Second, the two modes show similar porphyrin motions with the four pyrroles rotating opposite to the iron vibrations (ν50).44 It is worthy to note that two comparable Fe−NO bending modes, which also show orthogonal iron vibrations had been predicted at 574 and 580 cm−1 for the {FeNO}6 complex of [Fe(OEP)(NO)(2MeHIm)]ClO4. The trans 2-MeHIm has provided a ligand plane to distinguish the two modes.22 This is contrasted to the current case that the axial CCl2 itself serving as the ligand plane for the orientational measurements. Both x and y measurements observed peaks at 423, which are predicted at 428 and 431 cm−1, respectively. Both modes involves strong pyrrole and Fe−Npyrrole translation in opposite directions which are very comparable to the modes of 410 and 413 cm−1 in [Fe(TPP)(NO)].45 The two modes at 322 and 354 cm−1 are compared in Figure S4, which show very similar vibrations not only for the iron, two chlorine atoms, but also for porphyrin core atoms (ν53). Interestingly, pairs of modes in x and y directions are found to show similar vibrational features. The modes at 250 (x) and 255 (y) are observed at 256 and 260 cm−1, respectively, both showing characters of γ23.46 The modes at 223 (x) and 217 (y) are observed at 208 cm−1; both modes show strong pyrroles translation. The remaining modes including 345 (y), 298 (y), and 190 cm−1 (x) are given in Figure S5−S7 for comparison. Table 1 lists values for overall force constants extracted from the experimental VDOS in each direction.18 The stiffness is
Two special in plane measurements, either parallel (x) or perpendicular (y) to the axial CCl2 plane, were conducted. The experimental (green or red) and predicted (black) VDOS are given in the two panels of Figure 5. The bending mode, which
Table 1. Experimental Force Constants Determined from Fe-Weighted VDOS of [Fe(TTP)(CCl2)] along Three Orthogonal Directions
Figure 5. Measured (green or red) and DFT predicted (black) VDOS of [Fe(TTP)(CCl2)] along the direction of in plane x (top) or y (bottom).
direction
stiffness (pN/pm)
resilience (pN/pm)
x y z
302 ± 2 292 ± 10 335 ± 7
13.8(1) 13.8(1) 12.2(1)
proportional to the mean squared frequency (weighted by the Fe VDOS) and provides a direct measure of coordination strength, which does not depend on modeling the character of individual vibrational modes. Stiffness values for all three directions lie in the 280−370 pN/pm range previously observed for low-spin Fe porphyrins but are nonetheless significantly larger for the z direction. Smaller differences between the two in-plane directions are not statistically significant. The resilience is a distinct force constant, determined by the mean inverse squared frequency, which quantifies the elasticity of the matrix in which the iron is embedded. In contrast with the stiffness, the resilience is significantly smaller in the axial direction, although in-plane values are identical. Low frequencies (
