Unusually Stable Synthetic Diheme Bis-Fe(IV)oxo: An Intermediate in Diheme Enzymes MauG and BthA

Widespread diheme enzymes MauG and BthA of the bacterial cytochrome c peroxidase (bCCP) superfamily produce an unusually stable bis-Fe(IV) intermediate upon 2e¯-oxidation. Herein, we report, for the first time, the synthesis and characterization of the unusually stable bis-Fe(IV)═O intermediate, as a synthetic mimic of the bis-Fe(IV) species generated in the catalytic cycle of the native diheme enzymes that display similar stability at room temperature. Various spectroscopic techniques, including UV–vis, ESI-MS, EPR, resonance Raman, and Mössbauer, were utilized to thoroughly characterize this fairly stable intermediate. The reaction of a diiron(III) porphyrin dimer with soluble iodosylbenzene (^sPhIO) at −80 °C produces a red-colored solution of a hitherto unknown six-coordinate bis-Fe(III)porphyrin-^sPhIO adduct which quickly undergoes O–I bond cleavage to yield the green bis-Fe(IV)═O intermediate. The reactivities of such a bis-Fe(IV)═O intermediate have also been demonstrated in the oxygen atom transfer (OAT) and C–H bond activation reactions. Computational studies revealed that the local electric field (LEF) of one heme exerted on the other heme unit is most likely the root cause of the unusual stability of the bis-Fe(IV)═O complex reported here. Indeed, the bis-Fe(IV)═O intermediate has been found to be stabilized significantly relative to its monomeric unit, and the stability of the dimeric system is maximized when the two porphyrin planes are relatively oriented by 20°, at which the LEF reaches its maximum value. The present work provides an excellent opportunity for the mechanistic investigation of the highly challenging and unexplored diheme enzymatic processes and will therefore have widespread practical applicability.