Spectroscopic and Computational Study of a Nonheme Iron Nitrosyl Center in a Biosynthetic Model of Nitric Oxide Reductase

Chakraborty, Saumen; Reed, Julian H.; Ross, Matthew O.; Nilges, Mark J.; Petrík, Igor; Ghosh, Soumya; Hammes‐Schiffer, Sharon; Sage, J. Timothy; Zhang, Yong; Schulz, Charles E.; Lu, Yi

doi:10.1002/anie.201308431

Cited by 44 publications

(57 citation statements)

References 54 publications

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“…have concluded that the investigated S =3/2 {FeNO} 7 species can be described as a HS ( S =2) ferrous Fe II antiferromagnetically coupled with NO ( S =

1 / 2

) . The same conclusion was drawn from a recent spectroscopic and computational study of a non‐heme iron‐ nitrosyl center in a biosynthetic model of nitric oxide reductase …”

Section: Introductionsupporting

confidence: 74%

Electronic Structure Modulation in an Exceptionally Stable Non‐Heme Nitrosyl Iron(II) Spin‐Crossover Complex

Piñeiro‐López

Ortega-Villar

Muñoz

et al. 2016

Chemistry A European J

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The highly stable nitrosyl iron(II) mononuclear complex [Fe(bztpen)(NO)](PF6 )2 (bztpen=N-benzyl-N,N',N'-tris(2-pyridylmethyl)ethylenediamine) displays an S=1/2↔S=3/2 spin crossover (SCO) behavior (T1/2 =370 K, ΔH=12.48 kJ mol(-1) , ΔS=33 J K(-1) mol(-1) ) stemming from strong magnetic coupling between the NO radical (S=1/2) and thermally interconverted (S=0↔S=2) ferrous spin states. The crystal structure of this robust complex has been investigated in the temperature range 120-420 K affording a detailed picture of how the electronic distribution of the t2g -eg orbitals modulates the structure of the {FeNO}(7) bond, providing valuable magneto-structural and spectroscopic correlations and DFT analysis.

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“…have concluded that the investigated S =3/2 {FeNO} 7 species can be described as a HS ( S =2) ferrous Fe II antiferromagnetically coupled with NO ( S =

1 / 2

) . The same conclusion was drawn from a recent spectroscopic and computational study of a non‐heme iron‐ nitrosyl center in a biosynthetic model of nitric oxide reductase …”

Section: Introductionsupporting

confidence: 74%

Electronic Structure Modulation in an Exceptionally Stable Non‐Heme Nitrosyl Iron(II) Spin‐Crossover Complex

Piñeiro‐López

Ortega-Villar

Muñoz

et al. 2016

Chemistry A European J

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“…Since the CV signals from redox-active heme iron could interfere with those of the nonheme metal, we replaced heme with redox-inactive Zn protoporphyrin to obtain Fe B Mb(Zn II ) using a previously reported protocol. 31 The titration of Fe II and Cu I metals into the Fe B center of Fe B Mb(Zn II ) resulted in similar changes in the Soret and visible bands of the UV-Vis spectra, suggesting similar coordination environments of nonheme Fe II and Cu I in Fe B Mb(Zn II ) (Supplementary Fig. S6).…”

Section: Resultsmentioning

confidence: 88%

Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases

et al. 2016

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Heme-copper oxidase (HCO) catalyzes the natural reduction of oxygen to water using a heme-copper center. Despite decades of research on HCO's, the role of nonheme metal and Nature's choice of copper over other metals like iron remains unclear. Here, we use a biosynthetic model of HCO in myoglobin that selectively binds different nonheme metals to demonstrate 30-fold and 11-fold enhancements in oxidase activity of Cu- and Fe-bound HCO mimics respectively, as compared to Zn-bound mimics. Detailed electrochemical, kinetic and vibrational spectroscopic studies, in tandem with theoretical DFT calculations demonstrate that the nonheme metal not only donates electrons to oxygen but also activates it for efficient O-O bond cleavage. Furthermore, the higher redox potential of copper and the enhanced weakening of O-O bond from the higher electron density in the d-orbital of copper are central to its higher oxidase activity over iron. This work resolves a long-standing question in bioenergetics, and renders a chemical-biological basis for designing future oxygen reduction catalysts.

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“…Moreover, no synthetic model of NOR exhibits more than a single turnover of NO reduction. In this work, we utilize a myoglobin (Mb)-based structural and functional model of NOR (23)(24)(25)(26)(27)(28) to investigate the impact of tuning heme E°′ on NOR functionality. The structural simplicity of Mb makes it amenable to a variety of modulations for redox tuning: the H-bonding interaction to the proximal ligand of the heme iron can be readily tuned in Mb through site-directed mutagenesis of nearby amino acid residues (29).…”

Section: Significancementioning

confidence: 99%

Heme redox potentials hold the key to reactivity differences between nitric oxide reductase and heme-copper oxidase

Bhagi‐Damodaran

Reed

Zhu

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

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Despite high structural homology between NO reductases (NORs) and heme-copper oxidases (HCOs), factors governing their reaction specificity remain to be understood. Using a myoglobin-based model of NOR (FeMb) and tuning its heme redox potentials (E°') to cover the native NOR range, through manipulating hydrogen bonding to the proximal histidine ligand and replacing heme with monoformyl (MF-) or diformyl (DF-) hemes, we herein demonstrate that the E°' holds the key to reactivity differences between NOR and HCO. Detailed electrochemical, kinetic, and vibrational spectroscopic studies, in tandem with density functional theory calculations, demonstrate a strong influence of heme E°' on NO reduction. Decreasing E°' from +148 to -130 mV significantly impacts electronic properties of the NOR mimics, resulting in 180- and 633-fold enhancements in NO association and heme-nitrosyl decay rates, respectively. Our results indicate that NORs exhibit finely tuned E°' that maximizes their enzymatic efficiency and helps achieve a balance between opposite factors: fast NO binding and decay of dinitrosyl species facilitated by low E°' and fast electron transfer facilitated by high E°'. Only when E°' is optimally tuned in FeMb(MF-heme) for NO binding, heme-nitrosyl decay, and electron transfer does the protein achieve multiple (>35) turnovers, previously not achieved by synthetic or enzyme-based NOR models. This also explains a long-standing question in bioenergetics of selective cross-reactivity in HCOs. Only HCOs with heme E°' in a similar range as NORs (between -59 and 200 mV) exhibit NOR reactivity. Thus, our work demonstrates efficient tuning of E°' in various metalloproteins for their optimal functionality.

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Spectroscopic and Computational Study of a Nonheme Iron Nitrosyl Center in a Biosynthetic Model of Nitric Oxide Reductase

Cited by 44 publications

References 54 publications

Electronic Structure Modulation in an Exceptionally Stable Non‐Heme Nitrosyl Iron(II) Spin‐Crossover Complex

Electronic Structure Modulation in an Exceptionally Stable Non‐Heme Nitrosyl Iron(II) Spin‐Crossover Complex

Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases

Heme redox potentials hold the key to reactivity differences between nitric oxide reductase and heme-copper oxidase

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