Heme−Copper−Dioxygen Complexes: Toward Understanding Ligand-Environmental Effects on the Coordination Geometry, Electronic Structure, and Reactivity

Abstract

The nature of the ligand is an important aspect of controlling structure and reactivity in coordination chemistry. In connection with our study of heme/copper/oxygen reactivity relevant to cytochrome c oxidase O 2 -reduction chemistry, we compare the molecular and electronic structure of two highspin heme-peroxo-copper [Fe III -O 2 2--Cu II ] + complexes containing N 4 -tetradentate (1) or N 3 -tridentate (2) copper ligands. Combining previously reported and new resonance Raman and EXAFS data coupled to DFT calculations we report a geometric structure and more complete electronic description of the high-spin heme-peroxo-copper complexes 1 and 2, which establish μ-(O 2 2-) sideon to the Fe III and end-on to Cu II (μ-η 2 :η 1 ) binding for the complex 1 but side-on/side-on (μ-η 2 :η 2 ) μ-peroxo coordination for the complex 2. We also compare and summarize the differences and similarities of these two complexes in their reactivity toward CO, PPh 3 , acid and phenols. The comparison of a new X-ray structure of μ-oxo complex 2a with the previously reported 1a X-ray structure, two thermal decomposition products respectively of 2 and 1, reveals a considerable difference in the Fe-O-Cu angle between the two μ-oxo complexes (∠Fe-O-Cu = 178.2° in 1a, ∠Fe-O-Cu = 149.5° in 2a). The reaction of 2 with one equivalent of exogenous N-donor axial base leads to the formation of a distinctive low-temperature stable, low-spin heme-O 2 -Cu complex (2b), but under the same conditions the addition of an axial base to 1 leads to the dissociation of the hemeperoxo-Cu assembly and the release of O 2 . 2b reacts with phenols performing hydrogen-atom (e -+ H + ) abstraction resulting in O-O bond cleavage and the formation of high-valent ferryl [Fe IV =O] complex (2c). The nature of 2c was confirmed by comparison of its spectroscopic features and reactivity with those of an independently prepared ferryl complex. The phenoxyl radical generated by the hydrogen-atom abstraction was either 1) directly detected by EPR spectroscopy using phenols that produce stable radicals or 2) indirectly by detection of the coupling product of two phenoxyl radicals.karlin@jhu.edu, edward.solomon@stanford.edu. Supporting Information Available. UV-visible spectra of the reaction of (2b) with 1 equiv. of 2,4-di-tertbutylphenol ( Figure S1), UVvis spectra of the reaction of [(F 8 )Fe III -(O 2 2-)-Cu II (TMPA)] + (1) with DMAP ( Figure S2), EPR spectra of (2b) reaction with 1 equiv.of 2,4-di-tert-butylphenol ( Figure S3), GC-MS trace of the oxidative coupling of 2,4-di-tert-butylphenol in presence of (2b) ( Figure S4), ORTEP diagram ( Figure S5) and crystal data and structure refinement for [(F 8 )Fe III -(O 2-)-Cu II (AN)] + (2a) X-ray structure (Table S1), XAS spectra and computational data.NIH Public Access

Transition Metal Complexes and the Activation of Dioxygen

“…Further study of complexes 40 and 42 by DFT calculations showed this decrease in ν(O-O) to be the result of efficient backbonding from the copper center into the σ* orbital of the peroxo ligand in the case of the η 2 :η 2 binding configuration. Given the conformational restraints of the copper supporting ligand for compound 40, such backbonding does not occur [130]. Axial ligation at the heme center has also been demonstrated to have an effect on the binding mode of the peroxo bridge.…”

Respiratory Conservation of Energy with Dioxygen: Cytochrome c Oxidase

“…-OH À and a phenol radical ( Figure 12) [44]. Thus, in order to reduce the bound peroxide in the compounds given in Figure 12, the tridentate Cu complex stabilizes Figure 12 Formation of a phenoxy radical by addition of a phenol derivative to the heme-peroxy-tridentate copper complex (2b).…”

“…Thus, in order to reduce the bound peroxide in the compounds given in Figure 12, the tridentate Cu complex stabilizes Figure 12 Formation of a phenoxy radical by addition of a phenol derivative to the heme-peroxy-tridentate copper complex (2b). Reproduced by permission from [44]; copyright 2010 American Chemical Society. the low-spin state which has reactivity towards the phenolic OH group.…”

“…For example, the tridentate (trigonal planar) structure of Cu B is a prerequisite for stabilizing the Fe 3+ -O À 2 state [27]. The copper structure is also critical for the facile electron transfer to the peroxide-bridged intermediates by stabilizing the low spin hemeperoxide-copper state [44]. Thus, the peroxide-bridged intermediates are undetectable in the normal enzyme catalytic cycle.…”

“…Thus, the peroxide-bridged intermediates are undetectable in the normal enzyme catalytic cycle. Furthermore, various model compounds suggest the requirement of Tyr244 as electron donor to the bound O 2 [27,44].…”