No abstract

Nitric oxide (NO) is an important signaling molecule that is involved in a wide range of physiological and pathological events in biology. Metal coordination chemistry, especially with iron, is at the heart of many biological transformations involving NO. A series of heme proteins, nitric oxide synthases (NOS), soluble guanylate cyclase (sGC), and nitrophorins, are responsible for the biosynthesis, sensing, and transport of NO. Alternatively, NO can be generated from nitrite by heme- and copper-containing nitrite reductases (NIRs). The NO-bearing small molecules such as nitrosothiols and dinitrosyl iron complexes (DNICs) can serve as an alternative vehicle for NO storage and transport. Once NO is formed, the rich reaction chemistry of NO leads to a wide variety of biological activities including reduction of NO by heme or non-heme iron-containing NO reductases and protein post-translational modifications by DNICs. Much of our understanding of the reactivity of metal sites in biology with NO and the mechanisms of these transformations has come from the elucidation of the geometric and electronic structures and chemical reactivity of synthetic model systems, in synergy with biochemical and biophysical studies on the relevant proteins themselves. This review focuses on recent advancements from studies on proteins and model complexes that not only have improved our understanding of the biological roles of NO but also have provided foundations for biomedical research and for bio-inspired catalyst design in energy science.

Flavodiiron nitric oxide reductases (FNORs), a common enzyme family found in various types of pathogenic bacteria, are capable of reducing nitric oxide (NO) to nitrous oxide (NO) as a protective detoxification mechanism. Utilization of FNORs in pathogenic bacteria helps them survive and proliferate in the human body, thus causing chronic infections. In this paper, we present a new diiron model complex, [Fe((PyPhO)MP)(OPr)](OTf), with bridging propionate ligands (OPr) that is capable of directly reducing NO to NO in quantitative yield without the need to (super)reduce the complex. We first prepared the diferric precursor and characterized it by UV-vis, IR, NMR and Mössbauer spectroscopies, cyclic voltammetry, and mass spectrometry. This complex can then conveniently be reduced to the diferrous complex using CoCp. Even though this diferrous complex is highly reactive, we have successfully isolated and characterized this species using X-ray crystallography and various spectroscopic techniques. Most importantly, upon reacting this diferrous complex with NO gas, we observe quantitative formation of NO via IR gas headspace analysis, the first demonstration of direct NO reduction by a non-heme diiron model complex. This finding directly supports recent mechanistic proposals for FNORs.

The chemistry of nonheme iron centers with NO in different oxidation states has experienced a renaissance in the last 10 years because of recent findings of their involvement in N2O generation (in nitric oxide reductases – NORs), dinitrosyl iron complex (DNIC) formation, NO sensing in transcription factors, and the biosynthesis of natural products that contain N-nitroso groups. Using model complexes, great strides have been made in our understanding of the reactivity and electronic structures of nonheme iron-nitrosyl complexes in different oxidation states, and yet there is much more to be learned. Whereas many nonheme, high-spin (hs) {FeNO}7 complexes, formed from the reaction of NO with Fe­(II), have been prepared and thoroughly characterized (although even in this case, their ability to directly couple two NO to N2O in dinuclear systems had been overlooked for a long time), much less is known about nonheme iron-nitrosyl complexes in other oxidation states, especially hs-{FeNO}6 and hs-{FeNO}8. In both of these cases, very few examples have been reported, and the reactivity of these complexes is largely unexplored. This is an exciting area of coordination chemistry that warrants more attention in the field.

The intermediacy of metal–NNH2 complexes has been implicated in the catalytic cycles of several examples of transition-metal-mediated nitrogen (N2) fixation. In this context, we have shown that triphosphine-supported Fe­(N2) complexes can be reduced and protonated at the distal N atom to yield Fe­(NNH2) complexes over an array of charge and oxidation states. Upon exposure to further H+/e– equivalents, these species either continue down a distal-type Chatt pathway to yield a terminal iron­(IV) nitride or instead follow a distal-to-alternating pathway resulting in N–H bond formation at the proximal N atom. To understand the origin of this divergent selectivity, herein we synthesize and elucidate the electronic structures of a redox series of Fe­(NNMe2) complexes, which serve as spectroscopic models for their reactive protonated congeners. Using a combination of spectroscopies, in concert with density functional theory and correlated ab initio calculations, we evidence one-electron redox noninnocence of the “NNMe2” moiety. Specifically, although two closed-shell configurations of the “NNR2” ligand have been commonly considered in the literatureisodiazene and hydrazido(2−)we provide evidence suggesting that, in their reduced forms, the present iron complexes are best viewed in terms of an open-shell [NNR2]•– ligand coupled antiferromagnetically to the Fe center. This one-electron redox noninnocence resembles that of the classically noninnocent ligand NO and may have mechanistic implications for selectivity in N2 fixation activity.