The Spectroscopy of Nitrogenases

Stappen, Casey Van; Decamps, Laure; Cutsail, George E.; Björnsson, Ragnar; Henthorn, Justin T.; Birrell, James A.; DeBeer, Serena

doi:10.1021/acs.chemrev.9b00650

Cited by 155 publications

(174 citation statements)

References 650 publications

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“…Although these are plausibly attributed to one-electron-oxidized P-clusters, some debate remains about the origin of these signals. 28 …”

Section: Introductionmentioning

confidence: 99%

Quantum Mechanics/Molecular Mechanics Study of Resting-State Vanadium Nitrogenase: Molecular and Electronic Structure of the Iron–Vanadium Cofactor

Benediktsson

Björnsson

2020

Inorg. Chem.

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The nitrogenase enzymes are responsible for all biological nitrogen reduction. How this is accomplished at the atomic level, however, has still not been established. The molybdenum-dependent nitrogenase has been extensively studied and is the most active catalyst for dinitrogen reduction of the nitrogenase enzymes. The vanadium-dependent form, on the other hand, displays different reactivity, being capable of CO and CO 2 reduction to hydrocarbons. Only recently did a crystal structure of the VFe protein of vanadium nitrogenase become available, paving the way for detailed theoretical studies of the iron–vanadium cofactor (FeVco) within the protein matrix. The crystal structure revealed a bridging 4-atom ligand between two Fe atoms, proposed to be either a CO 3 2– or NO 3 – ligand. Using a quantum mechanics/molecular mechanics model of the VFe protein, starting from the 1.35 Å crystal structure, we have systematically explored multiple computational models for FeVco, considering either a CO 3 2– or NO 3 – ligand, three different redox states, and multiple broken-symmetry states. We find that only a [VFe 7 S 8 C(CO 3 )] 2– model for FeVco reproduces the crystal structure of FeVco well, as seen in a comparison of the Fe–Fe and V–Fe distances in the computed models. Furthermore, a broken-symmetry solution with Fe2, Fe3, and Fe5 spin-down (BS7-235) is energetically preferred. The electronic structure of the [VFe 7 S 8 C(CO 3 )] 2– BS7-235 model is compared to our [MoFe 7 S 9 C] − BS7-235 model of FeMoco via localized orbital analysis and is discussed in terms of local oxidation states and different degrees of delocalization. As previously found from Fe X-ray absorption spectroscopy studies, the Fe part of FeVco is reduced compared to FeMoco, and the calculations reveal Fe5 as locally ferrous. This suggests resting-state FeVco to be analogous to an unprotonated E 1 state of FeMoco. Furthermore, V–Fe interactions in FeVco are not as strong compared to Mo–Fe interactions in FeMoco. These clear differences in the electronic structures of otherwise similar cofactors suggest an explanation for distinct differences in reactivity.

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“…Although these are plausibly attributed to one-electron-oxidized P-clusters, some debate remains about the origin of these signals. 28 …”

Section: Introductionmentioning

confidence: 99%

Quantum Mechanics/Molecular Mechanics Study of Resting-State Vanadium Nitrogenase: Molecular and Electronic Structure of the Iron–Vanadium Cofactor

Benediktsson

Björnsson

2020

Inorg. Chem.

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“…It is notable that H 2 is a compulsory by-product. The mechanism of the nitrogenases has been extensively studied by biochemical, kinetic, spectroscopic and computational methods [ 1 , 5 , 7 – 9 ]. However, many details of the mechanism are still unknown.…”

Section: Introductionmentioning

confidence: 99%

Does the crystal structure of vanadium nitrogenase contain a reaction intermediate? Evidence from quantum refinement

2020

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Recently, a crystal structure of V-nitrogenase was presented, showing that one of the µ2 sulphide ions in the active site (S2B) is replaced by a lighter atom, suggested to be NH or NH2, i.e. representing a reaction intermediate. Moreover, a sulphur atom is found 7 Å from the S2B site, suggested to represent a storage site for this ion when it is displaced. We have re-evaluated this structure with quantum refinement, i.e. standard crystallographic refinement in which the empirical restraints (employed to ensure that the final structure makes chemical sense) are replaced by more accurate quantum–mechanical calculations. This allows us to test various interpretations of the structure, employing quantum–mechanical calculations to predict the ideal structure and to use crystallographic measures like the real-space Z-score and electron-density difference maps to decide which structure fits the crystallographic raw data best. We show that the structure contains an OH−-bound state, rather than an N2-derived reaction intermediate. Moreover, the structure shows dual conformations in the active site with ~ 14% undissociated S2B ligand, but the storage site seems to be fully occupied, weakening the suggestion that it represents a storage site for the dissociated ligand. Graphic abstract

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“…itrogenase, as a catalytic enzyme that reduces atmospheric dinitrogen to bioavailable ammonia in nature, has attracted widespread attentions from researchers [1][2][3][4][5] . Molybdenum nitrogenase consists of FeMo-and Fe-proteins, where FeMo-cofactor (FeMo-co) in FeMo-protein is the active site of substrate binding and reduction.…”

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confidence: 99%

Assignment of protonated R-homocitrate in extracted FeMo-cofactor of nitrogenase via vibrational circular dichroism spectroscopy

et al. 2020

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Protonation of FeMo-cofactor (FeMo-co) is important for the process of substrate hydrogenation. Its structure has been clarified as Δ-Mo*Fe7S9C(R-homocit*)(cys)(Hhis) after the efforts of nearly 30 years, but it remains controversial whether FeMo-co is protonated or deprotonated with chelated ≡C − O(H) homocitrate. We have used protonated molybdenum(V) lactate 1 and its enantiomer as model compounds for R-homocitrate in FeMo-co of nitrogenase. Vibrational circular dichroism (VCD) spectrum of 1 at 1051 cm−1 is attributed to ≡C − OH vibration, and molybdenum(VI) R-lactate at 1086 cm−1 is assigned as ≡C − Oα-alkoxy vibration. These vibrations set up labels for the protonation state of coordinated α-hydroxycarboxylates. The characteristic VCD band of NMF-extracted FeMo-co is assigned to ν(C − OH), which is based on the comparison of molybdenum(VI) R-homocitrate. Density functional theory calculations are consistent with these assignments. To the best of our knowledge, this is the first time that protonated R-homocitrate in FeMo-co is confirmed by VCD spectra.

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The Spectroscopy of Nitrogenases

Cited by 155 publications

References 650 publications

Quantum Mechanics/Molecular Mechanics Study of Resting-State Vanadium Nitrogenase: Molecular and Electronic Structure of the Iron–Vanadium Cofactor

Quantum Mechanics/Molecular Mechanics Study of Resting-State Vanadium Nitrogenase: Molecular and Electronic Structure of the Iron–Vanadium Cofactor

Does the crystal structure of vanadium nitrogenase contain a reaction intermediate? Evidence from quantum refinement

Assignment of protonated R-homocitrate in extracted FeMo-cofactor of nitrogenase via vibrational circular dichroism spectroscopy

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