5 Metal centers in hydrogenase enzymes studied by X-ray spectroscopy

Haumann, Michael

doi:10.1515/9783110336733.97

Cited by 4 publications

(2 citation statements)

References 89 publications

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“…Nuclear resonance scattering (NRS) is a synchrotron-based spectroscopic technique relying on the Mössbauer effect, that is, resonant excitation of 57 Fe nuclei using ∼14.4 keV X-rays. − The excitation creates a 1s level photoelectron due to nuclear excited state decay followed by core hole refill from higher electron levels (e.g., Fe-2p) and X-ray fluorescence photon emission (e.g., Fe Kα at ∼6.4 keV), which is employed to monitor the NRS effects in a time-resolved (nanoseconds) detection scheme including a high-resolution (meV) monochromator. Site-selective studies on the H-cluster are facilitated by the exclusive 57 Fe sensitivity of NRS. ,,,− Nuclear forward scattering (NFS) probes coherent emission interference during decay (lifetime 141 ns) of the I 1/2 and I 3/2 57 Fe excited nuclear spin levels to access Mössbauer parameters (quadrupole splitting energy, Δ E Q , and line width, Γ) . Nuclear resonance vibrational spectroscopy (NRVS) probes excitation or annihilation of phonons in the Stokes or anti-Stokes energy regions close to the 57 Fe resonance to monitor vibrational modes. ,,, NRVS is versatile because it is not limited by the Raman or infrared spectroscopy selection rules, but shows all modes with 57 Fe ion contributions, thereby probing the primary iron-ligand vibrations as well as cofactor-protein modes.…”

Section: Introductionmentioning

confidence: 99%

Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by ⁵⁷Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses

Mebs¹,

Duan²,

Wittkamp³

et al. 2019

Inorg. Chem.

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FeFe]-hydrogenases are efficient biological hydrogen conversion catalysts and blueprints for technological fuel production. The relations between substrate interactions and electron/proton transfer events at their unique six-iron cofactor (H-cluster) need to be elucidated. The H-cluster comprises a four-iron cluster, [4Fe4S], linked to a diiron complex, [FeFe]. We combined 57 Fe-specific X-ray nuclear resonance scattering experiments (NFS, nuclear forward scattering; NRVS, nuclear resonance vibrational spectroscopy) with quantum-mechanics/molecular-mechanics computations to study the [FeFe]-hydrogenase HYDA1 from a green alga. Selective 57 Fe labeling at only [4Fe4S] or [FeFe], or at both subcomplexes was achieved by protein expression with a 57 Fe salt and in vitro maturation with a synthetic diiron site precursor containing 57 Fe. H-cluster states were populated under infrared spectroscopy control. NRVS spectral analyses facilitated assignment of the vibrational modes of the cofactor species. This approach revealed the H-cluster structure of the oxidized state (Hox) with a bridging carbon monoxide at [FeFe] and ligand rearrangement in the CO-inhibited state (Hox-CO). Protonation at a cysteine ligand of [4Fe4S] in the oxidized state occurring at low pH (HoxH) was indicated, in contrast to bridging hydride binding at [FeFe] in a one-electron reduced state (Hred). These findings are direct evidence for differential protonation either at the four-iron or diiron subcomplex of the H-cluster. NFS time-traces provided Mossbauer parameters such as the quadrupole splitting energy, which differ among cofactor states, thereby supporting selective protonation at either subcomplex. In combination with data for reduced states showing similar [4Fe4S] protonation as HoxH without (Hred′) or with (Hhyd) a terminal hydride at [FeFe], our results imply that coordination geometry dynamics at the diiron site and proton-coupled electron transfer to either the four-iron or the diiron subcomplex discriminate catalytic and regulatory functions of [FeFe]-hydrogenases. We support a reaction cycle avoiding diiron site geometry changes during rapid H 2 turnover.

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Section: Introductionmentioning

confidence: 99%

Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by ⁵⁷Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses

Mebs¹,

Duan²,

Wittkamp³

et al. 2019

Inorg. Chem.

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“…23 Determination of cofactor protonation states in both cofactors is required to understanding the O 2 and cross-link formation chemistry. 22,24 We used advanced X-ray spectroscopy techniques, X-ray absorption (XAS) and emission (XES) spectroscopies, and nuclear resonance vibrational spectroscopy (NRVS, also called nuclear inelastic scattering, NIS), 25 to site-selectively probe the molecular and electronic configurations, ligand protonation states, and vibrational properties of the Mn(III) and Fe(III) ions in the MnFe and FeFe cofactors in R2lox. X-ray absorption near-edge spectroscopy (XANES) spectra at the Mn and Fe Kedges were used to determine metal oxidation states.…”

Section: ■ Introductionmentioning

confidence: 99%

Protonation State of MnFe and FeFe Cofactors in a Ligand-Binding Oxidase Revealed by X-ray Absorption, Emission, and Vibrational Spectroscopy and QM/MM Calculations

et al. 2016

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Enzymes with a dimetal-carboxylate cofactor catalyze reactions among the top challenges in chemistry such as methane and dioxygen (O) activation. Recently described proteins bind a manganese-iron cofactor (MnFe) instead of the classical diiron cofactor (FeFe). Determination of atomic-level differences of homo- versus hetero-bimetallic cofactors is crucial to understand their diverse redox reactions. We studied a ligand-binding oxidase from the bacterium Geobacillus kaustophilus (R2lox) loaded with a FeFe or MnFe cofactor, which catalyzes O reduction and an unusual tyrosine-valine ether cross-link formation, as revealed by X-ray crystallography. Advanced X-ray absorption, emission, and vibrational spectroscopy methods and quantum chemical and molecular mechanics calculations provided relative Mn/Fe contents, X-ray photoreduction kinetics, metal-ligand bond lengths, metal-metal distances, metal oxidation states, spin configurations, valence-level degeneracy, molecular orbital composition, nuclear quadrupole splitting energies, and vibrational normal modes for both cofactors. A protonation state with an axial water (HO) ligand at Mn or Fe in binding site 1 and a metal-bridging hydroxo group (μOH) in a hydrogen-bonded network is assigned. Our comprehensive picture of the molecular, electronic, and dynamic properties of the cofactors highlights reorientation of the unique axis along the Mn-OH bond for the Mn1(III) Jahn-Teller ion but along the Fe-μOH bond for the octahedral Fe1(III). This likely corresponds to a more positive redox potential of the Mn(III)Fe(III) cofactor and higher proton affinity of its μOH group. Refined model structures for the Mn(III)Fe(III) and Fe(III)Fe(III) cofactors are presented. Implications of our findings for the site-specific metalation of R2lox and performance of the O reduction and cross-link formation reactions are discussed.

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The binuclear nickel center in the A-cluster of acetyl-CoA synthase (ACS) and two biomimetic dinickel complexes studied by X-ray absorption and emission spectroscopy

Schrapers

Mebs

Ilina

et al. 2016

J. Phys.: Conf. Ser.

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5 Metal centers in hydrogenase enzymes studied by X-ray spectroscopy

Cited by 4 publications

References 89 publications

Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by ⁵⁷Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses

Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by ⁵⁷Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses

Protonation State of MnFe and FeFe Cofactors in a Ligand-Binding Oxidase Revealed by X-ray Absorption, Emission, and Vibrational Spectroscopy and QM/MM Calculations

The binuclear nickel center in the A-cluster of acetyl-CoA synthase (ACS) and two biomimetic dinickel complexes studied by X-ray absorption and emission spectroscopy

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5 Metal centers in hydrogenase enzymes studied by X-ray spectroscopy

Cited by 4 publications

References 89 publications

Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by 57Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses

Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by 57Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses

Protonation State of MnFe and FeFe Cofactors in a Ligand-Binding Oxidase Revealed by X-ray Absorption, Emission, and Vibrational Spectroscopy and QM/MM Calculations

The binuclear nickel center in the A-cluster of acetyl-CoA synthase (ACS) and two biomimetic dinickel complexes studied by X-ray absorption and emission spectroscopy

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Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by ⁵⁷Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses

Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by ⁵⁷Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses