Iron Dioxygen Adduct Formed during Electrochemical Oxygen Reduction by Iron Porphyrins Shows Catalytic Heme Dioxygenase Reactivity

Heme dioxygenases oxidize the indole ring of tryptophan to kynurenine which is the first step in the biosynthesis of several important biomolecules like NAD, xanthurenic acid, and picolinic acid. A ferrous heme dioxygen adduct (or Fe-III-O-2(center dot-)) is the oxidant, and both the atoms of O-2 are inserted in the product and its catalytic function has been difficult to emulate as it is complicated by competing rapid reactions like auto-oxidation and/or formation of the mu-oxo dimer. In situ resonance Raman spectroscopy technique, SERRS-RDE, is used to probe the species accumulated during electrochemical ORR catalyzed by site-isolated imidazole-bound iron porphyrin installed on a self-assembled monolayer covered electrode. These in situ SERRS-RDE data using labeled O-2 show that indeed a Fe-III-O-2(center dot-) species accumulate on the electrode during ORR between -0.05 and -0.30 V versus Ag/AgCl (satd. KCl) and is reduced by proton coupled electron transfer to a Fe-III-OOH species which, on the other hand, builds up on the electrode between -0.20 and -0.40 V versus Ag/AgCl (satd. KCl). This Fe-III-OOH species then gives way to a Fe-IV & boxH;O species, which accumulates at -0.50 V versus Ag/AgCl (satd. KCl). When 2,3-dimethylindole is present in the solution and the applied potential is held in the range where Fe-III-O-2(center dot-) species accumulate, it gets oxidized to N-(2-acetylphenyl)acetamide retaining both the oxygens from O-2 mimicking the reaction of heme dioxygenases. Turnover numbers more than 10(4) are recorded, establishing this imidazole-bound ferrous porphyrin as a functional model of heme dioxygenases.

Automated summary

Heme dioxygenases play a crucial role in the biosynthesis of important biomolecules. In this study, the catalytic function of a ferrous heme dioxygen adduct was investigated using in situ resonance Raman spectroscopy. The results showed the accumulation of different species during the electrochemical ORR catalysis, mimicking the reaction of heme dioxygenases. This study provides important insights into the mechanism of biological catalysts and can inspire the design of more efficient artificial catalysts.