Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase

@article{Shomura2011StructuralBF,
  title={Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase},
  author={Yasuhito Shomura and Ki Seok Yoon and Hirofumi Nishihara and Yoshiki Higuchi},
  journal={Nature},
  year={2011},
  volume={479},
  pages={253-256}
}
Membrane-bound respiratory [NiFe]-hydrogenase (MBH), a H2-uptake enzyme found in the periplasmic space of bacteria, catalyses the oxidation of dihydrogen: H2 → 2H+ + 2e− (ref. 1). In contrast to the well-studied O2-sensitive [NiFe]-hydrogenases (referred to as the standard enzymes), MBH has an O2-tolerant H2 oxidation activity; however, the mechanism of O2 tolerance is unclear. Here we report the crystal structures of Hydrogenovibrio marinus MBH in three different redox conditions at… 
The structural plasticity of the proximal [4Fe3S] cluster is responsible for the O2 tolerance of membrane-bound [NiFe] hydrogenases.
TLDR
EPR and FTIR studies on ReMBH and AaHase-1 have shown that, with the exception of the Ni-A species, most redox states observed in standard hydrogenases are also observed in these O2-tolerant enzymes.
Redox-dependent structural transformations of the [4Fe-3S] proximal cluster in O2-tolerant membrane-bound [NiFe]-hydrogenase: a DFT study.
Broken-symmetry density functional theory (BS-DFT) has been used to address the redox-dependent structural changes of the proximal [4Fe-3S] cluster, implicated in the O2-tolerance of membrane-bound
Proton Transfer Pathways between Active Sites and Proximal Clusters in the Membrane-Bound [NiFe] Hydrogenase.
TLDR
This work sequentially applies multiscale modeling techniques as quantum mechanical/molecular mechanics methods and classical molecular dynamics simulations to investigate the role of two distinct proton transfer pathways connecting the [NiFe] active site and the [4Fe3S] proximal cluster of ReMBH in the protection mechanism against an oxygen attack.
Reversible [4Fe-3S] cluster morphing in an O(2)-tolerant [NiFe] hydrogenase.
TLDR
These investigations unraveled the redox-dependent and reversible occurence of an oxygen ligand located at a different iron and proposed that these transformations, reminiscent of those of the P-cluster of nitrogenase, enable the consecutive transfer of two electrons within a physiological potential range.
Electronic structure of the unique [4Fe-3S] cluster in O2-tolerant hydrogenases characterized by 57Fe Mössbauer and EPR spectroscopy
TLDR
Field-dependent 57Fe-Mössbauer and EPR data for Hase I are presented, which reveal the distribution of Fe valences and spin-coupling schemes for the iron–sulfur clusters, and demonstrate that the electronic structure of the [4 Fe-3S] core in its three oxidation states closely resembles that of corresponding conventional [4Fe-4S] cubanes, albeit with distinct differences for some individual iron sites.
EPR spectroscopic studies of the Fe-S clusters in the O2-tolerant [NiFe]-hydrogenase Hyd-1 from Escherichia coli and characterization of the unique [4Fe-3S] cluster by HYSCORE.
TLDR
The (14)N hyperfine couplings are conclusive evidence that Fe(4) is a valence-localized Fe(3+) in the superoxidized state, whose formation permits an additional electron to be transferred rapidly back to the active site during O(2) attack.
X-ray crystallographic and computational studies of the O2-tolerant [NiFe]-hydrogenase 1 from Escherichia coli
The crystal structure of the membrane-bound O2-tolerant [NiFe]-hydrogenase 1 from Escherichia coli (EcHyd-1) has been solved in three different states: as-isolated, H2-reduced, and chemically
Crystal structure of the O(2)-tolerant membrane-bound hydrogenase 1 from Escherichia coli in complex with its cognate cytochrome b.
TLDR
The 3.3 Å resolution structure of dimeric membrane-bound O(2)-tolerant hydrogenase 1 from Escherichia coli in a 2:1 complex with its physiological partner, cytochrome b, is reported, predicting rapid transfer of H(2)derived electrons between hydrogenase heterodimers.
The F₄₂₀-reducing [NiFe]-hydrogenase complex from Methanothermobacter marburgensis, the first X-ray structure of a group 3 family member.
TLDR
The crystal structure of FrhABG from Methanothermobacter marburgensis at 1.7Å resolution is reported and the structures of group 1 [NiFe]-hydrogenases, the only group structurally characterized yet, are compared.
Reactivation from the Ni-B state in [NiFe] hydrogenase of Ralstonia eutropha is controlled by reduction of the superoxidised proximal cluster.
TLDR
It is proposed that the [4Fe-3S] cluster plays a major role in protecting MBH by blocking the reversal of electron transfer to the [NiFe] active site, which would produce damaging radical oxygen species.
...
1
2
3
4
5
...

References

SHOWING 1-10 OF 48 REFERENCES
Spectroscopic Insights into the Oxygen-tolerant Membrane-associated [NiFe] Hydrogenase of Ralstonia eutropha H16*
This study provides the first spectroscopic characterization of the membrane-bound oxygen-tolerant [NiFe] hydrogenase (MBH) from Ralstonia eutropha H16 in its natural environment, the cytoplasmic
Characterization of a unique [FeS] cluster in the electron transfer chain of the oxygen tolerant [NiFe] hydrogenase from Aquifex aeolicus
TLDR
It is suggested that the (1 + /2+) redox couple serves the classical electron transfer reaction, whereas the superoxidation step is associated with a redox switch against oxidative stress.
A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase.
TLDR
The data indicate that the mechanism of O(2) tolerance relies on the reductive removal of oxygenic species guided by the unique architecture of the electron relay rather than a restricted access of O (2) to the active site.
The three-dimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough: a hydrogenase without a bridging ligand in the active site in its oxidised, "as-isolated" state.
TLDR
The three-dimensional structure of the [NiFeSe] Hase from Desulfovibrio vulgaris Hildenborough has been determined in its oxidised "as-isolated" form and it is reported that an extra sulfur atom is observed binding Ni and Se, leading to a SeCys conformation that shields the NiFe site from contact with oxygen.
A kinetic and thermodynamic understanding of O2 tolerance in [NiFe]-hydrogenases
TLDR
A kinetic and thermodynamic model is presented to account for O2 tolerance in Re MBH that may be more widely applied to other [NiFe]-hydrogenases.
[NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8 Å and modelling studies of its interaction with the tetrahaem cytochrome c3
TLDR
The lowest energy docking solutions were found to correspond to an interaction between the haem IV region in tetrahaem cytochrome c3 with the distal [4Fe-4S] cluster in [NiFe] hydrogenase, which should correspond to efficient electron transfer and be physiologically relevant.
Redox-dependent structural changes in the nitrogenase P-cluster.
TLDR
Observed redox-mediated structural changes of the P-cluster suggest a role for this cluster in coupling electron transfer and proton transfer in nitrogenase.
REDOX PROPERTIES OF THE METAL CENTERS IN THE MEMBRANE-BOUND HYDROGENASE FROM ALCALIGENES-EUTROPHUS CH34
For highly active preparations of the membrane-bound, respiratory chain-linked hydrogenase from Alcaligenes eutrophus strains H16 and CH34, 0.7 moles of nickel and approximately 10 moles of iron per
A Glutamate Is the Essential Proton Transfer Gate during the Catalytic Cycle of the [NiFe] Hydrogenase*
Kinetic, EPR, and Fourier transform infrared spectroscopic analysis of Desulfovibrio fructosovorans [NiFe] hydrogenase mutants targeted to Glu-25 indicated that this amino acid participates in proton
Oxygen Tolerance of the H2-sensing [NiFe] Hydrogenase from Ralstonia eutropha H16 Is Based on Limited Access of Oxygen to the Active Site*
TLDR
Evidence is presented that the shape and size of the intramolecular hydrophobic cavities leading to the [NiFe] active site of the regulatory hydrogenase are crucial for oxygen insensitivity, which offers a new strategy how to engineer oxygen-tolerant hydrogenases for biotechnological application.
...
1
2
3
4
5
...