Distortion of the [FeNO] 2 Core in Flavodiiron Nitric Oxide Reductase Models Inhibits N-N Bond Formation and Promotes Formation of Unusual Dinitrosyl Iron Complexes: Implications for Catalysis and Reactivity.

Flavodiiron nitric oxide reductases (FNORs) carry out the reduction of nitric oxide (NO) to nitrous oxide (N ₂ O), allowing infectious pathogens to mitigate toxic levels of NO generated in the human immune response. We previously reported the model complex [Fe ₂ (BPMP)(OPr)(NO) ₂ ](OTf) ₂ ( 1 , OPr ^- = propionate) that contains two coplanar NO ligands and that is capable of quantitative NO reduction to N ₂ O [White et al. J. Am. Chem. Soc. 2018 , 140 , 2562-2574]. Here we investigate, for the first time, how a distortion of the active site affects the ability of the diiron core to mediate N ₂ O formation. For this purpose, we prepared several analogues of 1 that contain two monodentate ligands in place of the bridging carboxylate, [Fe ₂ (BPMP)(X) ₂ (NO) ₂ ] ^3+/1+ ( 2-X ; X = triflate, 1-methylimidazole, or methanol). Structural data of 2-X show that without the bridging carboxylate, the diiron core expands, leading to elongated (O)N-N(O) distances (from 2.80 Å in 1 to 3.00-3.96 Å in 2-X ) and distorted (O)N-Fe-Fe-N(O) dihedral angles (from coplanarity (5.9°) in 1 to 52.9-85.1° in 2-X ). Whereas 1 produces quantitative amounts of N ₂ O upon one-electron reduction, N ₂ O production is substantially impeded in 2-X , to an initial 5-10% N ₂ O yield. The main products after reduction are unprecedented hs-Fe ^II /{Fe(NO) ₂ } ^9/10 dinitrosyl iron complexes (DNICs). Even though mononuclear DNICs are stable and do not show N-N coupling (since it is a spin-forbidden process), the hs-Fe ^II /{Fe(NO) ₂ } ^9/10 DNICs obtained from 2-X show unexpected reactivity and produce up to quantitative N ₂ O yields after 2 h. The implications of these results for the active site structure of FNORs are discussed.