Comparative electronic structures of nitrogenase FeMoco and FeVco

Rees, Julian A.; Björnsson, Ragnar; Kowalska, Joanna K.; Lima, Frederico A.; Schlesier, Julia; Sippel, Daniel; Weyhermüller, Thomas; Einsle, Oliver; Kovacs, Julie A.; DeBeer, Serena

doi:10.1039/c7dt00128b

Cited by 70 publications

(136 citation statements)

References 70 publications

(91 reference statements)

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“…The blue arrows point toward the rising edge and white line onsets as well as indicate the MMCT feature. Adapted from ref (19), published by The Royal Society of Chemistry. See open access article: .…”

Section: Resultsmentioning

confidence: 99%

Iron L_2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase

et al. 2017

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Herein, a systematic study of a series of molecular iron model complexes has been carried out using Fe L2,3-edge X-ray absorption (XAS) and X-ray magnetic circular dichroism (XMCD) spectroscopies. This series spans iron complexes of increasing complexity, starting from ferric and ferrous tetrachlorides ([FeCl4]−/2–), to ferric and ferrous tetrathiolates ([Fe(SR)4]−/2–), to diferric and mixed-valent iron–sulfur complexes [Fe2S2R4]2–/3–. This test set of compounds is used to evaluate the sensitivity of both Fe L2,3-edge XAS and XMCD spectroscopy to oxidation state and ligation changes. It is demonstrated that the energy shift and intensity of the L2,3-edge XAS spectra depends on both the oxidation state and covalency of the system; however, the quantitative information that can be extracted from these data is limited. On the other hand, analysis of the Fe XMCD shows distinct changes in the intensity at both L3 and L2 edges, depending on the oxidation state of the system. It is also demonstrated that the XMCD intensity is modulated by the covalency of the system. For mononuclear systems, the experimental data are correlated with atomic multiplet calculations in order to provide insights into the experimental observations. Finally, XMCD is applied to the tetranuclear heterometal–iron–sulfur clusters [MFe3S4]3+/2+ (M = Mo, V), which serve as structural analogues of the FeMoco and FeVco active sites of nitrogenase. It is demonstrated that the XMCD data can be utilized to obtain information on the oxidation state distribution in complex clusters that is not readily accessible for the Fe L2,3-edge XAS data alone. The advantages of XMCD relative to standard K-edge and L2,3-edge XAS are highlighted. This study provides an important foundation for future XMCD studies on complex (bio)inorganic systems.

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Section: Resultsmentioning

confidence: 99%

Iron L_2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase

et al. 2017

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“…When the pre-edge features were modeled by pseudo-Voigt line shapes (excluding contributions from riding edge transitions), a comparison of the HERFD pre-edge area to the TFY pre-edge area shows that HERFD intensities are higher by a factor of ~1.3. The observed spectral features correspond to 1s to 3d transitions 36–38 (at lowest energies, ~7110–7115 eV) with additional charge transfer contributions 35, 39 observed to higher energies (~7118 eV).…”

Section: Introductionmentioning

confidence: 92%

“…32–35 The MMOH Q spectra are interpreted versus parallel studies on the open- and closed-core model compounds shown in Scheme 2. HERFD XAS is measured by scanning through the metal K-edge and measuring the resultant 2p-to-1s Kα-fluorescence using a high resolution Bragg optic.…”

Section: Introductionmentioning

confidence: 99%

High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase

Castillo

Banerjee²,

Allpress³

et al. 2017

J. Am. Chem. Soc.

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Kα High-Energy Resolution Fluorescence Detected X-ray Absorption Spectroscopy (HERFD XAS) provides a powerful tool for overcoming the limitations of conventional XAS to identify the electronic structure and coordination environment of metalloprotein active sites. Herein, Fe Kα HERFD-XAS is applied to the diiron active site of soluble Methane Monooxygenase (sMMO) and to a series of high-valent diiron model complexes, including a “diamond core” [FeIV2(μ-O)2(L)2](ClO4)4] (3) and an “open core” [(O=FeIV–O–FeIV(OH)(L)2](ClO4)3 (4) (where, L = tris(3,5-dimethyl-4-methoxypyridyl-2-methyl)amine) (TPA*)). Pronounced differences in the HERFD XAS pre-edge energies and intensities are observed for the open vs. closed Fe2O2 cores in the model compounds. These differences are reproduced by time-dependent density functional theory (TDDFT) calculations and allow for the pre-edge energies and intensity to be directly correlated with the local active site geometric and electronic structure. A comparison of the model complex HERFD XAS data to that of MMOHQ (the key intermediate in methane oxidation) is supportive of an open core structure. Specifically, the large pre-edge area observed for MMOHQ may be rationalized by invoking an open core structure with a terminal FeIV=O motif, though further modulations of the core structure due to the protein environment cannot be ruled out. The present study, thus, motivates the need for additional experimental and theoretical studies to unambiguously assess the active site conformation of MMOHQ.

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“…Due to resolution limitations and the fact that homocitrate was severely truncated and approximated as a glycolate group in their study, the validity of this assignment was unclear. In previous studies 28,29,30,31,32 by one of us (RB) we have assigned the alkoxide group of the homocitrate as protonated but have not until now given a complete justification for this as the question of how well the protein environment is described surrounding the homocitrate remained unclear. The only exception to this is the 4ND8 crystal structure, recently published by Rees & Howard et al 85 which is a crystal structure solved under basic (pH 9.5) conditions, where the O-O distance is on average 2.77 Å as shown in Figure 6d.…”

Section: Protonation State Of Homocitratementioning

confidence: 99%

“…Recently Adamo 26 et al used QM/QM' calculations to propose new mechanisms and Ryde et al studied protonation states by QM/MM 27 . In previous articles by one of us (RB) we utilized large 225-atom cluster models in our studies of the spectroscopic properties of the FeMo cofactor 28,29,30,31,32 . Large cluster models become difficult to work with and require many constraints to keep the correct active site geometry and may not describe correctly the structural flexibility of the cofactor in the enzyme active site pocket.…”

Section: Introductionmentioning

confidence: 99%

QM/MM Study of the Nitrogenase MoFe Protein Resting State: Broken-Symmetry States, Protonation States, and QM Region Convergence in the FeMoco Active Site

2017

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Nitrogenase is one of the most fascinating enzymes in nature, being responsible for all biological nitrogen reduction. Despite decades of research it is among the enzymes in bioinorganic chemistry whose mechanism is the most poorly understood. The MoFe protein of nitrogenase contains an iron-molybdenum-sulfur cluster, FeMoco, where N 2 reduction takes place. The resting state of FeMoco has been characterized by crystallography, multiple spectroscopic techniques and theory (broken-symmetry density functional theory) and all heavy atoms are now characterized. The cofactor charge, however, has been controversial, the electronic structure has proved enigmatic and little is known about the mechanism. While many computational studies have been performed on FeMoco, few have taken the protein environment properly into account. In this study, we put forward QM/MM models of the MoFe protein from Azotobacter vinelandii, centered on FeMoco. By a detailed analysis of the FeMoco geometry and comparing to the atomic resolution crystal structure we conclude that only the [MoFe 7 S 9 C] 1-charge is a possible resting state charge. Further we find that, of the 3 lowest energy broken-symmetry solutions of FeMoco the BS7-235 spin isomer (where 235 refers to Fe atoms that are "spin-down") is the only one that can be reconciled with experiment. This is revealed by a comparison of the metal-metal distances in the experimental crystal structure, a rare case of spin-coupling phenomena being visible through the molecular structure. This could be interpreted as the enzyme deliberately stabilizing a specific electronic state of the cofactor, possibly for tuning specific reactivity on specific metal atoms. Finally, we show that the alkoxide group on the Mo-bound homocitrate must be protonated under resting state conditions; the presence of which has implications regarding the nature of FeMoco redox states as well as for potential substrate reduction mechanisms.3

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Comparative electronic structures of nitrogenase FeMoco and FeVco

Abstract: High-resolution X-ray spectroscopy provides insights into the electronic structural differences between the nitrogenase FeMoco and FeVco clusters.

Cited by 70 publications

References 70 publications

Iron L_2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase

Iron L_2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase

High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase

QM/MM Study of the Nitrogenase MoFe Protein Resting State: Broken-Symmetry States, Protonation States, and QM Region Convergence in the FeMoco Active Site

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Comparative electronic structures of nitrogenase FeMoco and FeVco

Abstract: High-resolution X-ray spectroscopy provides insights into the electronic structural differences between the nitrogenase FeMoco and FeVco clusters.

Cited by 70 publications

References 70 publications

Iron L2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase

Iron L2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase

High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase

QM/MM Study of the Nitrogenase MoFe Protein Resting State: Broken-Symmetry States, Protonation States, and QM Region Convergence in the FeMoco Active Site

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Iron L_2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase

Iron L_2,3-Edge X-ray Absorption and X-ray Magnetic Circular Dichroism Studies of Molecular Iron Complexes with Relevance to the FeMoco and FeVco Active Sites of Nitrogenase