Quantitative vibrational dynamics of iron in nitrosyl porphyrins

Abstract

We use quantitative experimental and theoretical approaches to characterize the vibrational dynamics of the Fe atom in porphyrins designed to model heme protein active sites. Nuclear resonance vibrational spectroscopy (NRVS) yields frequencies, amplitudes, and directions for 57Fe vibrations in a series of ferrous nitrosyl porphyrins, which provide a benchmark for evaluation of quantum chemical vibrational calculations. Detailed normal mode predictions result from DFT calculations on ferrous nitrosyl tetraphenylporphyrin Fe(TPP)(NO), its cation [Fe(TPP)(NO)]+, and ferrous nitrosyl porphine Fe(P)(NO). Differing functionals lead to significant variability in the predicted Fe-NO bond length and frequency for Fe(TPP)(NO). Otherwise, quantitative comparison of calculated and measured Fe dynamics on an absolute scale reveals good overall agreement, suggesting that DFT calculations provide a reliable guide to the character of observed Fe vibrational modes. These include a series of modes involving Fe motion in the plane of the porphyrin, which are rarely identified using infrared and Raman spectroscopies. The NO binding geometry breaks the four-fold symmetry of the Fe environment, and the resulting frequency splittings of the in-plane modes predicted for Fe(TPP)(NO) agree with observations. In contrast to expectations of a simple three-body model, mode energy remains localized on the FeNO fragment for only two modes, an N-O stretch and a mode with mixed Fe-NO stretch and FeNO bend character. Bending of the FeNO unit also contributes to several of the in-plane modes, but no primary FeNO bending mode is identified for Fe(TPP)(NO). Vibrations associated with hindered rotation of the NO and heme doming are predicted at low frequencies, where Fe motion perpendicular to the heme is identified experimentally at 73 and 128 cm-1. Identification of the latter two modes is a crucial first step toward quantifying the reactive energetics of Fe porphyrins and heme proteins.

Figure 1

Calculated structure of ferrous nitrosyl tetraphenylporphyrin, Fe(TPP)(NO), resulting from geometric optimization with the B3LYP functional and 6-31G* + VTZ basis set to minimize the molecular energy. Selected structural parameters are reported in Table 1.

Figure 2

Measured ⁵⁷Fe excitation probabilities for a series of iron porphyrins. All nitro-syl complexes have an Fe-NO stretch/bend mode in the 520 – 540 cm⁻¹ region. Comparison among the nitrosyl complexes (c-g) reveals that peripheral groups strongly influence the vibrational frequencies and amplitudes of the central Fe. Sample temperatures were 34 K for Fe(OEP), 30 K for Fe(OEP)(NO), 80 K for Fe(TPP)(NO), 35 K for Fe(DPIXDME)(NO), 34 K for Fe(PPIXDME)(NO), and 64 K for Fe(MPIXDME)(NO). The Fe(OEP)(Cl) spectrum is an average over multiple scans with an estimated average temperature of 87 K. Error bars reflect Poisson statistics.

Figure 3

Raman spectra of Fe(TPP)(NO) powders, showing elimination of 547 cm⁻¹ peak with increasing laser flux. Scattering from powder in a spinning NMR tube was excited at 413.1 nm, using laser powers of 0.1 mW and 10 mW.

Figure 4

Comparison of the experimental VDOS determined from NRVS measurements on Fe (TPP)(NO) (upper panel) with the VDOS predicted on the basis of DFT calculations using B3LYP (center panel) and BP86 (lower panel) functionals. Black traces represent the partial VDOS 3 $\langle D_{\widehat{k}}(\overline{\nu })\rangle$ for oriented crystals, scaled by a factor 3 for comparison with the total VDOS $D(\overline{\nu })$ of unoriented polycrystalline powder (red traces). Since the X-ray beam direction $\widehat{k}$ lies 6° from the porphyrin plane, modes involving Fe motion in the plane of the porphyrin are enhanced, and modes with Fe motion primarily normal to the plane are suppressed, in the scaled oriented crystal VDOS relative to the powder VDOS. Cross-hatching in the upper panel indicates the area attributable to acoustic modes. In the lower two panels, the Fe-NO stretch/bend modes, predicted at 386 cm⁻¹ and 623 cm⁻¹, have been artificially shifted to the observed 539 cm⁻¹ frequency to facilitate comparison with the experimental results. Predicted VDOS are convolved with a 10 cm⁻¹ Gaussian.

Figure 5

One-, two-, and three-phonon contributions to the vibrational excitation probability $S^{\prime }(\overline{\nu })$ for oriented crystals of Fe(TPP)(NO). At the 32 K temperature of the measurements, multiphonon contributions constitute less than 10% of the total integrated vibrational excitation probability.

Figure 6

Cumulative contribution of vibrational modes to the Fe VDOS predicted on the basis of B3LYP calculations on Fe(TPP)(NO), [Fe(TPP)(NO)]⁺, and Fe(P)(NO), and a BP86 calculation on Fe(TPP)(NO). Modes are ranked in decreasing order of $e_{Fe}^2$ The inset shows an expanded view for the first 20 modes. For Fe(TPP)(NO), 23 modes contribute 97% of the area of the total B3LYP-predicted VDOS.

Figure 7

Direct comparison of measured and predicted vibrational densities of states for Fe(TPP)(NO). The measured and calculated Fe-NO frequencies are indicated.

Figure 8

Predicted in-plane and out-of-plane contributions to the total Fe VDOS for Fe(TPP)(NO), [Fe(TPP)(NO)]⁺, and Fe(P)(NO), predicted on the basis of B3LYP calculations. The partial densities of states $D_{\perp }(\overline{\nu })$ perpendicular to the porphyrin plane and $D_{\left|\right|}(\overline{\nu })$ parallel to the porphyrin plane contribute to the total VDOS $D(\overline{\nu })$ Gaussian line shape functions $L(\overline{\nu }-{\overline{\nu }}_{\alpha })$ with 8 cm⁻¹ FWHM are used in Eqs. 7 and 6 to approximate the resolution of the experimental data.

Figure 9

Comparison of vibrational dynamics of Fe and the nitrosyl N and O atoms for Fe(TPP)(NO), [Fe(TPP)(NO)]⁺, and Fe(P)(NO), predicted on the basis of B3LYP calculations. The heights of the individual bars indicate the fraction of mode energy associated with each of these three atoms. These stick spectra reveal fine structure that is not apparent after convolution with a lineshape function, as in Fig. 7.

Figure 10

Four in-plane Fe modes, predicted on the basis of B3LYP calculations, contributing to the pair of experimental features at 312 cm⁻¹ and 333 cm⁻¹ in the Fe(TPP)(NO). Arrows represent the mass-weighted displacements of the individual atoms. For ease of visualization, each arrow is 100(m_j/m_Fe)^1/2 times longer than the zero point vibrational amplitude of atom j. Color scheme: cyan–iron, green–carbon, blue–nitrogen, red–oxygen. In this and other figures, hydrogens are omitted for clarity.

Figure 11

Other modes with significant in-plane Fe motion, resulting from B3LYP calculations on Fe(TPP)(NO). Arrows representing mass-weighted atomic displacements are 100(m_j/m_Fe)^1/2 times longer than the zero point vibrational amplitudes. Color scheme as in Fig. 10.

Figure 12

Predicted Fe-NO stretch/bend modes for Fe(TPP)(NO), [Fe(TPP)(NO)]⁺, and Fe(P)(NO). For the linear FeNO fragment in [Fe(TPP)(NO)]⁺, the mode resembles a pure Fe-NO stretching modes. In contrast, the relative contribution of Fe-NO stretching and FeNO bending character differs considerably for the similar nonlinear FeNO fragments in Fe(TPP)(NO) and Fe(P)(NO). Note that an independent mode with FeNO bending character is not identified for the B3LYP calculation on Fe(TPP)(NO). Arrows representing mass-weighted atomic displacements are 100(m_j/m_Fe)^1/2 times longer than the zero point vibrational amplitudes. Color scheme as in Figs. 10 and 11.

Figure 13

Predicted low frequency Fe modes of Fe(TPP)(NO), resulting from B3LYP calculations. Modes at 27 cm⁻¹, 54 cm⁻¹, 77 cm⁻¹, and 109 cm⁻¹, respectively, primarily involve porphyrin core translation, Fe-NO torsion, FeNO bending, and Fe out-of-plane motion coupled to doming of the porphyrin core. Arrows representing mass-weighted atomic displacements are 100(m_j/m_Fe)^1/2 times longer than the zero point vibrational amplitudes. Color scheme as in Figs. 10–12.