Coordination of Diatomic Ligands to Heme: Simply CO

Abstract

The synthesis and molecular structures of three iron(II) porphyrinates with only CO as the axial ligand(s) are reported. Two five-coordinate [Fe(OEP)(CO)] derivatives have Fe–C = 1.7077 (13) and 1.7140 (10) Å, much shorter than those of six-coordinate [Fe(OEP)(Im)(CO)], although ν_C-O is 1944–1948 cm⁻¹. The six-coordinate species [Fe(OEP)(CO)₂] has also been studied. The competition for π-back-bonding of two CO ligands leads to Fe–C distances of 1.8558 (10) Å and ν_C-O is increased to 2021 cm⁻¹. The Mössbauer spectrum has a quadrupole splitting constant of 0 mm/s at 4.2 K, indicating high electronic symmetry.

Many heme-based sensing proteins that use/detect the diatomic ligands O₂, CO, or NO are known.^1–4 These sensing proteins rely on variations in coordination number and the character of their axial ligands to induce conformational changes leading to protein activation.¹ Effects involving the trans ligand (or lack thereof) on binding diatomic molecules are important in elucidating the mechanism of small-molecule-sensing proteins. In order to achieve a better understanding of the heme interactions involved with diatomic ligand sensing as well as broadly extending our understanding of their electronic and molecular structure, we have been investigating heme/diatomic ligand interactions.

We report for the first time the solid-state syntheses and structural characterization of unambiguously five-coordinate and six-coordinate heme CO complexes: [Fe(OEP)(CO)], [Fe(OEP)(CO)].C₆H₆, and [Fe(OEP)(CO)₂].^5,6 Although these species have been previously reported in solution and CO binding constants determined for three different porphyrins,⁷ we now demonstrate the structural effects of changing coordination environments. We compare the five-coordinate structures with those of several other diatomic ligand heme complexes, examine effects of the addition of a sixth ligand and note structural differences.

These adducts may elucidate important coordination chemistry features involving ligand loss, ligand switching, and ligand photolability. CO photolysis of six-coordinate heme carbonyl derivatives has been a mainstay in biophysical investigations,⁸ and is very efficient with quantum yields nearing unity. The suggestion that five-coordinate heme carbonyls are less photolabile than their six-coordinate counterparts⁹ generates important questions about structural differences.

We first consider the vibrational properties of five-coordinate [Fe(OEP)(CO)]. ν_C-O in unperturbed imidazole-ligated hemes is typically near 1970 cm⁻¹, but solid-state environmental factors can lead to variation in ν_C-O in the range of 1926 to 2000 cm^−1.10,11 Thus, it is perhaps surprising to find that ν_C-O in [Fe(OEP)(CO)] and [Fe(OEP)(CO)].C₆H₆ is well within this range at 1944 cm⁻¹ and 1948 cm⁻¹, respectively (Nujol mull). These values might suggest that the iron center is involved in a significant intermolecular interaction to form a pseudo six-coordinate complex, but this is not correct (vide infra).

The molecular structures of the two crystalline [Fe(OEP)(CO)] complexes are illustrated in Figure 1 (and Fig. S1). There are strong similarities as well as differences in their structures: the iron out-of-plane displacements are similar at 0.20 Å or 0.22 Å, the off-axis tilt of the Fe–C vector is 3.8° or 2.4°, and the Fe–C–O bond angle is 177.20(8)° in both. Both forms show some ring–ring interactions although these lead to some strong differences as well. Figure 2a shows the pairwise interactions in [Fe(OEP)(CO)], while the equivalent packing in the benzene solvate is shown in Figure 2b. In both cases, there is inversion symmetry; metrical information is given in the figure caption. The inter-ring packing pattern in the unsolvated form of [Fe(OEP)(CO)] (Figure 2a) is similar to that of both crystalline forms of [Fe(OEP)(NO)] for which little por-phyrin overlap is observed.¹² The closest intermolecular contact to the iron in [Fe(OEP)(CO)] is 3.12 Å whereas in [Fe(OEP)(CO)].C₆H₆ the closest contact to iron is 3.58 Å. In the two [Fe(OEP)(NO)]⁺ structures (isoelectronic to the CO's), however, there is a large porphyrin ring overlap with the π-system of an adjacent molecule acting as a pseudo sixth ligand.¹³ The tighter interactions in [Fe(OEP)(CO)].C₆H₆ (Figure 2b) are comparable although slightly larger than in the isoelectronic [Fe(OEP)(NO)]⁺ complexes. The porphyrin core conformation in [Fe(OEP)(CO)] is nearly planar whereas that in [Fe(OEP)(CO)].C₆H₆ displays modest core ruffling. The average equatorial Fe–Np distances are 1.988 (2) Å and 1.984(3) Å for the unsolvated and solvated forms. The very short Fe–N_p bond distances reflect the strong bonding interaction and low-spin state of iron. Significantly, the axial ligand-induced equatorial (Fe–N_p) bond distance differences observed in five-coordinate [Fe(por)(NO)] derivatives¹² are not observed; individual Fe–Np distances are tightly clustered.

Figure 1.

Thermal ellipsoid plot of [Fe(OEP)(CO)] (50% probability ellipsoids). Hydrogen atoms are omitted for clarity.

Figure 2.

ORTEP plots (50% probability ellipsoids) of [Fe(OEP)(CO)] (a) and [Fe(OEP)(CO)].C₆H₆ (b) displaying the pairwise interactions. In (a) the 24-atom mean plane separation is 3.42 Å and the lateral shift of the two ring centers is 6.76 Å. The Fe^…Fe distance is 7.58 Å. The corresponding distances in (b) are 3.46, 3.88, and 5.20 Å, respectively.

The short axial Fe–C distance of 1.7140(11) Å in [Fe(OEP)(CO)] is shorter than those of the six-coordinate imidazole adducts by ~0.03–0.06 Å.^10,14 This might suggest stronger Fe→C π-back-donation, but the relatively normal ν_C-O value suggests that the Fe π-donation into the CO π* orbitals is similar to that of the six-coordinate species. This would then suggest that it is the σ-bonding component that leads to the shorter Fe–C bond distance. The distance in [Fe(OEP)(CO)].C₆H₆ is 1.7077 (13) Å; the possibly slightly shorter Fe–C distance is not consistent with the 4 cm⁻¹ increase in ν_C-O, again suggesting the importance of σ-bonding. We thus conclude that differences in the σ-bonding component of Fe–C have no or modest effects on ν_C-O. As we have noted for a different series of six-coordinate carbonyl derivatives,¹⁰ there is a strong correlation between ν_C-O and the Fe–C/C–O bond lengths, this question is being examined in more detail for OEP derivatives.

The structures of other [Fe(OEP)(XY)]^{+, 0} adducts (XY = NO or CS) are available for comparison. Structural parameters for five- and six-coordinate species are listed in Table 1. The iron out-of-plane displacement of [Fe(OEP)-(CO)] is seen to be at the low end of the range. In all cases, the addition of a sixth ligand leads to a decreased iron atom displacement and in most cases to an increase in the length of the Fe–X(XY) bond. Although this increase is never large, the COs are the system that experiences the largest increase in Fe–C bond distance (from 1.7140(11) Å to 1.7733(12) Å in [Fe(OEP)(CO)(1-MeIm)].¹⁴ Interestingly, the Fe–C bond would appear to have changed minimally when the trans ligand is the weakly coordinating tetrahydrofuran ligand in [Fe(Deut)(CO)(THF)]. Unfortunately, the relatively low precision of this structure (from ~25 years ago) is not adequate to comment on further, but clearly merits further attention.

Table 1.

Notable bonding parameters for [Fe(OEP)(CO)] and related compounds.

Complex	Fe–XYa	X–Ya	Fe–X–Yb	Fe–Npa	Fe–Laxa	ΔFed	νX–Yc	ref
[Fe(OEP)(CO)]	1.7140(11)	1.1463(12)	177.20(8)	1.988(2)	–	0.20	1944e	tw
[Fe(OEP)(CO)].C6H6	1.7077(13)	1.1259(16)	177.20(11)	1.984(3)	–	0.22	1948e	tw
[Fe(OEP)(NO)]	1.722(2)	1.167(3)	144.4(2)	2.004(15)	–	0.29	1666e	12
[Fe(OEP)(NO)]	1.7307(7)	1.1677(11)	142.74(8)	2.010(13)	–	0.27	1673e	12
[Fe(OEP)(NO)]+	1.6528(13)	1.140(2)	173.19(13)	1.994(5)	–	0.32	1838e	13
[Fe(OEP)(NO)]+	1.644(3)	1.112(4)	176.9(3)	1.994(1)	–	0.29	1868e	16
[Fe(OEP)(CS)]	1.662(3)	1.559(3)	176.3(2)	1.982(5)	–	0.23	1292e	17
[Fe(Deut)(CO)(THF)]	1.706(5)	1.144(5)	178.3(14)	1.98(3)	2.127(4)	0.10	1955f	18
[Fe(OEP)(CO)(1-MeIm)]	1.744(5)	1.158(5)	175.1(4)	2.000(3)	2.077(3)	0.00	1965g	19
[Fe(OEP)(CO)(1-MeIm)]	1.7733(12)	1.1413(15)	175.67(11)	2.010(4)	2.0544(9)	0.02	1980e	20
[Fe(OEP)(NO)(1-MeIm)]+	1.6465(17)	1.135(2)	177.28(17)	2.003(5)	1.9889(16)	0.02	1921e	21
[Fe(TPP)(NO)(1-MeIm)]	1.750(2)	1.182(3)	137.7(2)	2.008(13)	2.173(2)	0.04	1628e	22
[Fe(OEP)(CS)(1-MeIm)]	1.703(4)	1.563(4)	172.2(2)	2.001(4)	2.112(3)	0.10	1272e	23
[Fe(OEP)(CO)2]	1.8558(10)	1.1216(13)	173.95(9)	2.0133(7)	1.558(10)	0.00	2021e	tw

^aÅ

^bdegrees.

^ccm−1

^dDisplacement from 24-atom meanplane.

^eNujol mull.

^fTHF.

^gCD₂Cl₂ solution.

Although solutions of Fe(OEP) and CO will always be mixtures of mono- and bis-CO species, crystallization experiments (see SI) at low temperature reproducibly afford crystals of [Fe(OEP)(CO)₂]. Analysis of crystals of [Fe(OEP)(CO)₂] gave the structure displayed in Figure 3; the complex has a required inversion center. As might be expected, the competition from two COs for π-backbonding from the central iron leads to increased Fe–C bond distances of 1.8558 (10) Å, which is also consistent with the observed asymmetric stretch of 2021 cm⁻¹. The CO ligands are tilted off-axis as shown with other metrical information given in Figure 3. Perhaps as a consequence of the competition for bonding with two CO ligands, the equatorial Fe–N_p bonds are at the very long end of values expected for low-spin iron(II).¹⁵ The porphyrin core is planar; core diagrams for all three complexes are given in Figure S2.

Figure 3.

Thermal ellipsoid plot of [Fe(OEP)(CO)₂]. The Fe–C vector is tilted from the heme normal by 5.9°; the C and O atoms are shifted laterally by 0.14 and 0.56 Å, respectively.

Mössbauer spectra for [Fe(OEP)(CO)] are consistent with an isolated five-coordinate iron center. The quadrupole splitting is much larger (1.84 mm/s, 4.2 K) than that observed for six-coordinate carbonyls (typically less than 0.7 mm/s), strongly indicative of a d-orbital asymmetry consistent with five-coordination. The isomer shift value of 0.27 mm/s is similar to that of the six-coordinate derivatives; the relatively low value is consistent with strong and effectively equivalent covalency among the occupied Fe 3d orbitals in all derivatives. The six-coordinate derivative is much more symmetric with a quadrupole splitting of 0 or near 0 at 4.2 K and isomer shift of 0.31 mm/s, this increases to a QS of 0.176 mm/s and an isomer shift of 0.18 mm/s at 298 K. Spectra in applied magnetic field for this complex confirmed that it is a diamagnetic species. Complete data are in Table S1.

Five-coordinate coordinate carbonyl hemes have been structurally characterized and compared with related five- and six-coordinated diatomic complexes. Although the biological importance of five-coordinate carbonyl hemes is not known, proteins have been described that have spectroscopic properties that may be associated with this adduct.^9,24 Additional spectroscopic and photophysical studies on these carbonyl complexes are in prospect.