Dioxygen Binding to Protonated Heme in the Gas Phase, an Intermediate Between Ferric and Ferrous Heme

Abstract

With a view to characterizing the influence of the electronic structure of the Fe atom on the nature of its bond with dioxygen (O ) in heme compounds, a study of the UV/Vis action spectra and binding energies of heme-O molecules has been undertaken in the gas phase. The binding reaction of protonated ferrous heme [Fe -hemeH] with O has been studied in the gas phase by determining the equilibrium of complexed [Fe -hemeH(O )] with uncomplexed protonated heme in an ion trap at controlled temperatures. The binding energy of O to the Fe atom of protonated ferrous heme was obtained from a van't Hoff plot. Surprisingly, this energy (1540±170 cm , 18.4±2 kJ mol ) is intermediate between those of ferric heme and ferrous heme. This result is interpreted in terms of a delocalization of the positive charge over the porphyrin cycle, such that the Fe atom bears a fractional positive charge. The resulting electron distribution on the Fe atom differs notably from that of a purely low-spin ferrous heme [Fe -heme(O )] complex, as deduced from its absorption spectrum. It also differs from that of ferric heme [Fe -heme(O )] , as evidenced by the absorption spectra. Protonated heme creates a specific bond that cannot accommodate strong σ donation.

The dioxygen adducts of iron and manganese porphyrins: electronic structure and binding energy

“…We first showed that, as opposed to the end-on configuration of FeP−O 2 , MnP−O 2 prefers the side-on configuration. Our theoretical results predict a side-on quartet GS, in agreement with an early prediction of Basolo et al based on IR and EPR 17,19 and a more recent work of Gallagher et al 20 A detailed analysis of the GS wave function revealed a strong charge transfer between MnP and O 2 , leading to an assignment of O 2 somewhere 21,47 Our theoretical results are in perfect agreement with the experimental data, with errors less than 2 kcal/mol. Both the experimental and calculated data clearly indicate that O 2 binds more strongly by 4-6 kcal mol −1 to manganese porphyrin than to the corresponding ferrous porphyrin.…”

“…Consequently, the binding enthalpy in [FehemeH] + -O 2 is reduced by 4.3 kcal mol −1 as compared to the neutral porphyrin. We finally note that experiments 47 and our calculations both predict a small standard binding enthalpy of O 2 to [FehemeH] + (4-5 kcal mol −1 ).…”

“…This correction accounts for the fact that a substituent at either eight β -carbons or four meso-carbons can alter the O 2 binding energy. 28,47 The results are shown in Table 3. Two important trends can be seen from both theoretical and experimental results.…”

“…Motivated by the successful prediction of CASPT2 for the binding energy of FeP−O 2 , 8 we further calculate the binding energies of O 2 to both MnP and FeP. The calculated results will be compared with recent gas-phase experimental data by Karpuschkin et al 21 for [Fe II (tpps)] 4− and [Mn II (tpps)] 4− and Shafizadeh et al 47 for protonated ferrous heme 48 [Fe II hemeH] + (see Figure 2).…”

The dramatic effect of N-methylimidazole on trans axial ligand binding to ferric heme: experiment and theory

“…While solution measurements hardly access the observation of 5C hemes because of the blocking ligation to H2O (or the solvent), only gas phase measurements [7][8][9][10][11][12] render the sole or sequential addition of ligands in axial position to heme rather simple, by physically separating the ligation events and avoiding the spurious ligation by H2O (or the solvent). Following our recent studies on the binding of small ligands to ferric heme 11 and protonated heme 12 in a cold, temperature controlled, ion trap, we herein use the same approach with the presence of N- Indeed, the Fe III atom in the high spin state S=5/2 inflates due to electron repulsion and pops out of the porphyrin cage.…”