Quantitative Vibrational Dynamics of Iron in Carbonyl Porphyrins

Abstract

We use nuclear resonance vibrational spectroscopy and computational predictions based on density functional theory (DFT) to explore the vibrational dynamics of (57)Fe in porphyrins that mimic the active sites of histidine-ligated heme proteins complexed with carbon monoxide. Nuclear resonance vibrational spectroscopy yields the complete vibrational spectrum of a Mössbauer isotope, and provides a valuable probe that is not only selective for protein active sites but quantifies the mean-squared amplitude and direction of the motion of the probe nucleus, in addition to vibrational frequencies. Quantitative comparison of the experimental results with DFT calculations provides a detailed, rigorous test of the vibrational predictions, which in turn provide a reliable description of the observed vibrational features. In addition to the well-studied stretching vibration of the Fe-CO bond, vibrations involving the Fe-imidazole bond, and the Fe-N(pyr) bonds to the pyrrole nitrogens of the porphyrin contribute prominently to the observed experimental signal. All of these frequencies show structural sensitivity to the corresponding bond lengths, but previous studies have failed to identify the latter vibrations, presumably because the coupling to the electronic excitation is too small in resonance Raman measurements. We also observe the FeCO bending vibrations, which are not Raman active for these unhindered model compounds. The observed Fe amplitude is strongly inconsistent with three-body oscillator descriptions of the FeCO fragment, but agrees quantitatively with DFT predictions. Over the past decade, quantum chemical calculations have suggested revised estimates of the importance of steric distortion of the bound CO in preventing poisoning of heme proteins by carbon monoxide. Quantitative agreement with the predicted frequency, amplitude, and direction of Fe motion for the FeCO bending vibrations provides direct experimental support for the quantum chemical description of the energetics of the FeCO unit.

Spectroscopic identification of reactive porphyrin motions

“…11,[23][24][25][26][27][28][29][30] Since the use of NRVS to measure low frequency vibrations is restricted only by the experimental resolution (∼10 cm −1 ), it provides an important opportunity to characterize thermally excitable reactive modes. In particular, NRVS measurements have identified 11,[23][24][25]28 the doming mode of the heme (Fig. 1) long believed to control biologically important reactions in heme proteins, such as cooperative oxygen binding in hemoglobin.…”

“…In contrast, NRVS measurements on oriented single crystals definitively identify Fe motion orthogonal to the heme plane associated with low frequency modes in model compounds. 17,25,27,28,[48][49][50] In addition, NRVS represents the ultimate limit in atomic selectivity, because it specifically reveals the vibrational spectrum of the probe nucleus, even in the presence of thousands of other vibrating atoms. Fe-ligand vibrations dominate the 57 Fe NRVS signal.…”

“…25 Motion of the axial imidazole ligand contributes to multiple vibrations in six-coordinate iron carbonyl porphyrins. 28 Although quantum chemical calculations accurately reproduce the observed 57 Fe vibrations, 19,25,27,28 a more systematic approach is needed to interpret the predicted vibrational structure.…”

“…We find that removal of the peripheral substituents greatly simplifies the vibrational density of states (VDOS) of the Fe atom in comparison with those we reported for more complex porphyrins. 11,[23][24][25][26][27][28] A vibrational correlation method introduced here allows a simple description of the observed vibrations in terms of the mode nomenclature established for the four-coordinate Ni(P) molecule. 51 Halide binding reduces the symmetry from D 4h to C 4v , and the loss of the symmetry plane allows modest mixing between nominally inplane and out-of-plane modes.…”

Cis-dicarbonyl binding at cobalt and iron porphyrins with saddle-shape conformation

“…In the context of the discrimination between CO of endogenous origin and dioxygen many explanations invoke the local environment of the prosthetic group acting specifically on the ligated molecules via steric, hydrogen bonding or electrostatic interactions. 1,16,17,18 For the analysis it is generally assumed that monocarbonyl axial ligation takes place right at the metal center, 1 whereby distortions of the functional group may occur in the presence of the adduct. This calls for investigations probing directly the interaction of CO with model porphyrin systems, where the conformation of the macrocycle is controlled and a surrounding is provided that precludes the interference of additional protein or other units.…”