Co- and Counterrotation of Magnetic Axes and Axial Ligands in Low-Spin Ferriheme Systems

Abstract

The orientation of the principal axes of the g tensor with respect to the relationship of axial ligand planes to the porphyrin nitrogens has been studied in the framework of the one-electron crystal field model for tetragonal and rhombic low-spin d5 complexes such as ferriheme centers. All five d atomic orbitals were taken into account for two different ground-state electronic configurations, the “normal” (d xy )2(d xz ,d yz )3 and the “novel” (d xz ,d yz )4(d xy )1 configurations. The expressions for the g tensor, g values, and magnetic axes were derived on the basis of first-order perturbation theory. The conditions for co- and counterrotation of magnetic axes with rotation of planar axial ligands away from the porphyrin nitrogens toward the meso positions and beyond, as well as the order of g values, have been analyzed. It is found that counterrotation is the only possibility for the (d xz ,d yz )4(d xy )1 configuration and that it is also by far more common for the (d xy )2(d xz ,d yz )3 electron configuration. The possibilities of nonlinear co-/counterrotation are also explored. The predictions of this treatment are then compared to experimental results obtained from single-crystal EPR, glassy sample ESEEM, and solution NMR spectroscopic studies. It is clear that the majority of experimental systems reported thus far follow the major predictions of this treatment: Most systems exhibit angle-for-angle (linear) counterrotation of the g or χ tensor with rotation of planar axial ligands away for the N−Fe−N axes. Hence, knowing the structure of a model heme or heme protein, and in particular, the orientation of (fixed) axial ligand planes, one should be able to predict the approximate orientation of the in-plane magnetic axes. This knowledge provides a check on the values obtained in new solution NMR, single-crystal EPR or frozen solution ESEEM experiments.

Probing the heme-pocket structure of the paramagnetic forms of cytoglobin and a distal histidine mutant using electron paramagnetic resonance

“…This can only be the case when the two Fe-His bonds have a comparable strength [34,35]. This assignment is also corroborated by the fact that only one set of cross peaks between the double quantum (DQ) nuclear frequencies is found for the coordinating N ε of the two axially binding histidines (Figures 2a-b, 3a-b).…”

1H NMR Investigation of the Distal Hydrogen Bonding Network and Ligand Tilt in the Cyanomet Complex of Oxygen-avidAscaris suum Hemoglobin

“…The re-evaluation of the x-ray diffraction data to reconcile the alternate heme orientation in the crystal and solution has shown that the heme in the crystal is, in fact, rotated by 180°about the ␣,␥-meso axis from that originally reported (8) 4 and the same as found by 1 H NMR in solution. Theoretical considerations (61,64) confirmed in model compounds (65,66) dictate that if the orbital ground state is determined by the axial His(F8) bonding, the rhombic axes, , and the angle between the heme N-Fe-N and imidazole plane, (Fig. 1C), obey the counter-rotation rule where ϭ Ϫ.…”

Assignment of the Ferriheme Resonances of the High-Spin Forms of Nitrophorins 1 and 4 by 1H NMR Spectroscopy: Comparison to Structural Data Obtained from X-ray Crystallography

“…62 These angle plots are based on the contact shifts that measure the calculated spin density distributions in the e(π) orbital of the ferriheme for which the nodal plane of that orbital is coincident with the nodal plane of the axial ligand(s), 62 and the calculated pseudocontact shifts that depend on the orientation of the magnetic axes of the heme, with counter-rotation of ligand and x or y axes. 63 Table 1, and are compared to the orientation of the effective nodal plane of the histidine imidazole and the A:B ratios as determined by NMR spectroscopy in this work. The latter, and their relationship to the X-ray crystallographic data, are discussed below.…”