Synthetic Model Complex of the Key Intermediate in Cytochrome P450 Nitric Oxide Reductase

McQuarters, Ashley B.; Blaesi, Elizabeth J.; Kampf, Jeff W.; Alp, E. Ercan; Zhao, Jiyong; Hu, Michael; Krebs, Carsten; Lehnert, Nicolai

doi:10.1021/acs.inorgchem.8b02947

Synthetic Model Complex of the Key Intermediate in Cytochrome P450 Nitric Oxide Reductase

Journal Article · Wed Jan 09 00:00:00 EST 2019 · Inorganic Chemistry

DOI:https://doi.org/10.1021/acs.inorgchem.8b02947· OSTI ID:1509892

McQuarters, Ashley B. ^[1]; Blaesi, Elizabeth J. ^[2]; Kampf, Jeff W. ^[1]; Alp, E. Ercan ^[3]; Zhao, Jiyong ^[3]; Hu, Michael ^[3]; ^[2]; ^[1]

Univ. of Michigan, Ann Arbor, MI (United States)
The Pennsylvania State Univ., University Park, PA (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)

Fungal denitrification plays a crucial role in the nitrogen cycle and contributes to the total N₂O emission from agricultural soils. Here, cytochrome P450 NO reductase (P450nor) reduces two NO to N₂O using a single heme site. Despite much research, the exact nature of the critical "Intermediate I" responsible for the key N-N coupling step in P450nor is unknown. This species likely corresponds to a Fe-NHOH-type intermediate with an unknown electronic structure. Here we report a new strategy to generate a model system for this intermediate, starting from the iron(III) methylhydroxylamide complex [Fe(3,5-Me-BAFP)(NHOMe)] (1), which was fully characterized by ¹H NMR, UV-vis, electron paramagnetic resonance, and vibrational spectroscopy (rRaman and NRVS). Our data show that 1 is a high-spin ferric complex with an N-bound hydroxylamide ligand that is strongly coordinated (Fe–N distance, 1.918 Å; Fe-NHOMe stretch, 558 cm^–1). Simple one-electron oxidation of 1 at –80 °C then cleanly generates the first model system for Intermediate I, [Fe(3,5-Me-BAFP)(NHOMe)]⁺ (1⁺). UV–vis, resonance Raman, and Mössbauer spectroscopies, in comparison to the chloro analogue [Fe(3,5-Me-BAFP)(Cl)]⁺, demonstrate that 1⁺ is best described as an Fe^III-(NHOMe)• complex with a bound NHOMe radical. Further reactivity studies show that 1⁺ is highly reactive toward NO, a reaction that likely proceeds via N–N bond formation, following a radical–radical-type coupling mechanism. Here our results therefore provide experimental evidence, for the first time, that an Fe^III-(NHOMe)• electronic structure is indeed a reasonable electronic description for Intermediate I and that this electronic structure is advantageous for P450nor catalysis because it can greatly facilitate N–N bond formation and, ultimately, N₂O generation.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1509892

Journal Information:: Inorganic Chemistry, Journal Name: Inorganic Chemistry Journal Issue: 2 Vol. 58; ISSN 0020-1669

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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