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.

Vibrational dynamics of biological molecules: Multi-quantum contributions

“…Calculations were performed with Gaussian 98 [34], using the 6-31G basis set for N, O, C, and H atoms, Ahlrich's VTZ basis set for the Fe atom [35], and the Becke-Lee-Yang-Parr composite exchange correlation functional (B3LYP) [36,37]. Vibrational properties of the 91-atom molecule are determined from the relative Cartesian displacements of each atom for each of the 267 vibrational modes, as described previously [28].…”

“…The quantitative set of frequencies, amplitudes, and directions provided by NRVS rigorously test vibrational predictions for transition metals at protein active sites. In particular, DFT predictions were shown to be a useful guide to the vibrational modes observed in NRVS data for the model compound Fe(TPP)(NO) [28].…”

“…2 determines the areas of the features contributing to the predicted excitation probability shown in Fig. 2, using e 2 Fe values determined from the calculated atomic displacements, as discussed previously [28].…”

“…NRVS achieves the ultimate goal in selectivity, by targeting a single atom in a complex molecule. This method is particularly promising for characterizing the vibrational dynamics of 57 Fe in biological macromolecules [11,15,21,22,[25][26][27], and in small molecules designed to model protein active sites [16,19,20,24,28].…”

“…Measurements on oriented samples, such as single crystals, also yield the direction of vibrational motions [10,12,14,18,23,20,26,28]. Other names used for this technique include phonon assisted Mössbauer effect [21,22,25,26], inelastic X-ray scattering of synchrotron radiation [11], nuclear inelastic scattering [18], nuclear inelastic absorption [9], and nuclear resonant inelastic X-ray scattering [29].…”