Critical Aspects of Heme–Peroxo–Cu Complex Structure and Nature of Proton Source Dictate Metal–O_peroxo Breakage versus Reductive O–O Cleavage Chemistry

Abstract

The 4H+/4e− reduction of O2 to water, a key fuel-cell reaction also carried out in biology by oxidase enzymes, includes the critical O–O bond reductive cleavage step. Mechanistic investigations on active-site model compounds, which are synthesized by rational design to incorporate systematic variations, can focus on and resolve answers to fundamental questions, including protonation and/or H-bonding aspects, which accompany electron transfer. Here, we describe the nature and comparative reactivity of two low-spin heme–peroxo–Cu complexes, LS-4DCHIm, [(DCHIm)F8FeIII-(O22−)-CuII(DCHIm)4]+, and LS-3DCHIm, [(DCHIm)F8FeIII-(O22−)-CuII(DCHIm)3]+ (F8 = tetrakis(2,6-difluorophenyl)-porphyrinate; DCHIm = 1,5-dicyclohexylimidazole), toward different proton (4-nitrophenol and [DMF·H+](CF3SO3−)) (DMF = dimethylformamide) or electron (decamethylferrocene (Fc*)) sources. Spectroscopic reactivity studies show that differences in structure and electronic properties of LS-3DCHIm and LS-4DCHIm lead to significant differences in behavior. LS-3DCHIm is resistant to reduction, is unreactive toward weakly acidic 4-NO2–phenol, and stronger acids cleave the metal–O bonds, releasing H2O2. By contrast, LS-4DCHIm forms an adduct with 4-NO2–phenol, which includes an H-bond to the peroxo O-atom distal to Fe (resonance Raman (rR) spectroscopy and DFT). With addition of Fc* (2 equiv overall required), O–O reductive cleavage occurs, giving water, Fe(III), and Cu(II) products; however, a kinetic study reveals a one-electron rate-determining process, ket = 1.6 M−1 s−1 (−90 °C). The intermediacy of a high-valent [(DCHIm)F8FeIV = O] species is thus implied, and separate experiments show that one-electron reduction-protonation of [(DCHIm)F8FeIV=O] occurs faster (ket2 = 5.0 M−1 s−1), consistent with the overall postulated mechanism. The importance of the H-bonding interaction as a prerequisite for reductive cleavage is highlighted.

Mechanisms of Two‐Electron versus Four‐Electron Reduction of Dioxygen Catalyzed by Earth‐Abundant Metal Complexes

“…A low spin heme‐peroxo‐Cu complex ([(DCHIm)F 8 Fe III (O 2 2− )‐Cu II (DCHIm) 4 ] + ) (F 8 = tetrakis(2,6‐difluorophenyl)porphyrinate; DCHIm = 1,5‐dicyclohexylimidazole) prepared from a “naked” high‐spin heme‐peroxo‐Cu complex undergoes O−O bond cleavage when a weak phenolic acid such as 4‐nitrophenol is employed with an electron donor (Fc*), to produce Cu II OH and an iron(IV)‐oxo intermediate [Fe IV (O)] that was further reduced by Fc* with an acid to yield H 2 O along the Fe III and Cu II complexes (Scheme ) . The hydrogen bonding of 4‐nitrophenol with the peroxo moiety plays the key role for the O−O bond cleavage . In contrast, the addition of a strong acid such as [DMF‐H + ](CF 3 SO 3 − ) to a MeTHF solution of [(DCHIm)F 8 Fe III (O 2 2− )‐Cu II (DCHIm) 4 ] + resulted in the Fe−O bond cleavage to yield H 2 O 2 along the Fe III and Cu II complexes (Scheme ) .…”

“…The hydrogen bonding of 4‐nitrophenol with the peroxo moiety plays the key role for the O−O bond cleavage . In contrast, the addition of a strong acid such as [DMF‐H + ](CF 3 SO 3 − ) to a MeTHF solution of [(DCHIm)F 8 Fe III (O 2 2− )‐Cu II (DCHIm) 4 ] + resulted in the Fe−O bond cleavage to yield H 2 O 2 along the Fe III and Cu II complexes (Scheme ) . Thus, the two‐electron/two‐proton vs. four‐electron/four‐proton reduction of O 2 with C c O model complexes may be determined by the acidity of the acid source and the hydrogen bonding of the acid to the peroxo moiety of the heme‐peroxo‐Cu complex …”

“…[71] In contrast, the addition of as trong acid such as 4 ] + resulted in theF e ÀOb ond cleavage to yield H 2 O 2 along the Fe III and Cu II complexes (Scheme 2). [71] Thus, the two-electron/two-proton vs. four-electron/four-proton reduction of O 2 with CcOm odel complexes may be determined by the acidity of the acid source and the hydrogenb ondingo ft he acid to the peroxo moiety of the heme-peroxo-Cu complex. [71,72] Notably,t he selectivity of two-electron/two-protonv s. fourelectron/four-proton reduction of O 2 is highly dependento n the preparation method of the heterogeneousc atalysts.…”

“…[71] Thus, the two-electron/two-proton vs. four-electron/four-proton reduction of O 2 with CcOm odel complexes may be determined by the acidity of the acid source and the hydrogenb ondingo ft he acid to the peroxo moiety of the heme-peroxo-Cu complex. [71,72] Notably,t he selectivity of two-electron/two-protonv s. fourelectron/four-proton reduction of O 2 is highly dependento n the preparation method of the heterogeneousc atalysts. [73] Thus, general conclusions on the selectivity of two-electron/ two-proton vs. four-electron/four-proton reduction of O 2 must be tested by using multiple immobilizationm ethods ande lectrocatalysis conditions, whichs hould also be compared with the homogeneous catalytic transformation.…”

Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O2 Reduction in Heme–Copper Oxidases

“…Electrons are delivered to the active site through a low-spin, bis-His-ligated heme cofactor (heme a ) found in all HCOs, and C c O additionally contains a binuclear Cu center (Cu A ) responsible for mediating electron transfer (ET) from cytochrome c to heme a . While the presence of these additional metal centers complicates data from many spectroscopic methods, the use of model chemistry (including generation of key species whose interrogation can shed light on questions of particular and important concern), 8 site-selective spectroscopies, and computational studies provide promising means of studying the 4H + /4e − reduction of O 2 to H 2 O by the BNC.…”