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Structural insight into metallocofactor maturation in carbon monoxide dehydrogenase.

Elizabeth C Wittenborn1, Steven E Cohen1, Mériem Merrouch2

  • 1Department of Chemistry, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139.

The Journal of Biological Chemistry
|July 13, 2019
PubMed
Summary

Nickel insertion into the carbon monoxide dehydrogenase (CODH) C-cluster requires the maturation factor CooC and a functional D-cluster. An empty nickel site alone is insufficient for nickel incorporation into this metalloenzyme.

Keywords:
X-ray crystallographybioremediation catalystcarbon monoxide dehydrogenase (CODH)heterometallic cofactoriron–sulfur proteinmetalloenzymenickelone-carbon metabolismoxidation-reduction (redox)

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Area of Science:

  • Biochemistry
  • Structural Biology
  • Enzymology

Background:

  • Carbon monoxide dehydrogenase (CODH) is a metalloenzyme crucial for carbon cycling.
  • CODH utilizes a nickel-iron-sulfur cluster (C-cluster) for CO/CO2 interconversion.
  • The mechanism of nickel insertion into the C-cluster, dependent on the CooC maturation factor, is poorly understood.

Purpose of the Study:

  • To elucidate the mechanism of nickel insertion into the CODH C-cluster.
  • To investigate the roles of the maturation factor CooC and the D-cluster in CODH assembly.
  • To determine the structural requirements for nickel incorporation into the C-cluster.

Main Methods:

  • X-ray crystallography of Desulfovibrio vulgaris CODH (DvCODH) variants.
  • Heterologous expression of DvCODH in the presence and absence of CooC.
  • Structural comparison of C-clusters with varying iron and nickel occupancy.

Main Results:

  • CODH expressed without CooC contained iron but no nickel in the C-cluster, with iron occupying the nickel site.
  • A DvCODH variant lacking the D-cluster also failed to incorporate nickel, despite CooC presence.
  • The D-cluster-deficient CODH was inactive and could not be reconstituted with nickel.

Conclusions:

  • Nickel incorporation into the CODH C-cluster requires both CooC and a functional D-cluster.
  • An empty nickel site is insufficient for nickel insertion; precise redox control and a two-step process are likely involved.
  • A proposed model highlights the essential roles of CooC, the D-cluster, and redox state in C-cluster assembly.