The extended reductive acetyl-CoA pathway: ATPases in metal cluster maturation and reductive activation

Jeoung, Jae‐Hun; Goetzl, Sebastian; Hennig, Sandra E.; Fesseler, Jochen; Wörmann, C; Dendra, Julia; Dobbek, Holger

doi:10.1515/hsz-2013-0290

Cited by 18 publications

(12 citation statements)

References 92 publications

(144 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Previous studies have shown that integration of nickel into the C-cluster is dependent on the accessory protein CooC (15)(16)(17). Certain organisms express additional proteins, CooJ and CooT, that have been implicated in C-cluster maturation; however, CooC appears to be the only dedicated and essential maturation factor expressed by all CODH-containing organisms (15,(18)(19)(20)(21)(22). CooC is a P-loop ATPase with sequence similarity to UreG and HypB, maturation factors involved in nickel transfer to the active sites of urease and Ni-Fe hydrogenase, respectively (15,23).…”

Section: Introductionmentioning

confidence: 99%

Structural insight into metallocofactor maturation in carbon monoxide dehydrogenase

Wittenborn

Cohen

Merrouch

et al. 2019

Journal of Biological Chemistry

View full text Add to dashboard Cite

The nickel-dependent carbon monoxide dehydrogenase (CODH) employs a unique heterometallic Ni-Fe-S cluster, termed the C-cluster, to catalyze the interconversion of CO and CO2. Like other complex metalloenzymes, CODH requires dedicated assembly machinery to form the fully intact and functional C-cluster. In particular, nickel incorporation into the C-cluster depends on the maturation factor CooC; however, the mechanism of nickel insertion remains poorly understood. Here, we compare X-ray structures (1.50-2.48 Å resolution) of CODH from Desulfovibrio vulgaris (DvCODH) heterologously expressed in either the absence (DvCODH −CooC) or presence (DvCODH +CooC) of co-expressed CooC. We find that the C-cluster of DvCODH −CooC is fully loaded with iron but does not contain any nickel. Interestingly, the so-called unique iron ion (Feu) occupies both its canonical site (80% occupancy) and the nickel site (20% occupancy), with addition of reductant causing further mismetallation of the nickel site (60% iron occupancy). We also demonstrate that a DvCODH variant that lacks a surface-accessible Fe-S cluster (the D-cluster) has a C-cluster that is also replete in iron but lacks nickel, despite co-expression with CooC. In this variant, all Feu is in its canonical location and the nickel site is empty. This D-cluster-deficient CODH is inactive despite attempts to reconstitute it with nickel. Taken together, these results suggest that an empty nickel site is not sufficient for nickel incorporation. Based on our findings, we propose a model for C-cluster assembly that requires both CooC and a functioning D-cluster, involves precise redox-state control, and includes a two-step nickel-binding process.

show abstract

Section: Introductionmentioning

confidence: 99%

Structural insight into metallocofactor maturation in carbon monoxide dehydrogenase

Wittenborn

Cohen

Merrouch

et al. 2019

Journal of Biological Chemistry

View full text Add to dashboard Cite

show abstract

“…Several biological carbon dioxide (CO 2 ) to biomass conversion pathways exist in prokaryotes and eukaryotes [ 8 ]. Various prokaryotes employ the Wood-Ljungdahl pathway to reductively form acetyl coenzyme-A [ 9 , 10 ]. Carbon monoxide (CO) as obtained from CO 2 reduction by CO dehydrogenase (CODH) is utilized in a reaction involving two enzymes, corrinoid iron-sulfur protein (CoFeSP) with a methyl group bound to the cobalt ion of its cobalamin cofactor and acetyl-CoA synthase (ACS), to produce acetyl-CoA, the central metabolic building block ( Eq 1 ) [ 11 – 14 ].…”

Section: Introductionmentioning

confidence: 99%

Ligand binding at the A-cluster in full-length or truncated acetyl-CoA synthase studied by X-ray absorption spectroscopy

et al. 2017

Self Cite

View full text Add to dashboard Cite

Bacteria integrate CO2 reduction and acetyl coenzyme-A (CoA) synthesis in the Wood-Ljungdal pathway. The acetyl-CoA synthase (ACS) active site is a [4Fe4S]-[NiNi] complex (A-cluster). The dinickel site structure (with proximal, p, and distal, d, ions) was studied by X-ray absorption spectroscopy in ACS variants comprising all three protein domains or only the C-terminal domain with the A-cluster. Both variants showed two square-planar Ni(II) sites and an OH- bound at Ni(II)p in oxidized enzyme and a H2O at Ni(I)p in reduced enzyme; a Ni(I)p-CO species was induced by CO incubation and a Ni(II)-CH3- species with an additional water ligand by a methyl group donor. These findings render a direct effect of the N-terminal and middle domains on the A-cluster structure unlikely.

show abstract

“…Cbl is essential for all mammals [ 5 ] and in bacteria it is involved in carbon oxide (CO x ) conversion pathways related to potential renewable energy applications [ 6 , 7 ]. Anaerobic CO 2 reduction along the bacterial Wood-Ljungdahl pathway includes several unique enzymes [ 8 , 9 ]. The corrinoid iron-sulfur protein (CoFeSP) carries a Cbl cofactor [ 10 , 11 ] and shuttles a methyl group from methyl-transferase bound methyl-tetrahydrofolate to acetyl-CoA synthase.…”

Section: Introductionmentioning

confidence: 99%

Axial Ligation and Redox Changes at the Cobalt Ion in Cobalamin Bound to Corrinoid Iron-Sulfur Protein (CoFeSP) or in Solution Characterized by XAS and DFT

Schrapers¹,

Mebs²,

Goetzl³

et al. 2016

PLoS ONE

Self Cite

View full text Add to dashboard Cite

A cobalamin (Cbl) cofactor in corrinoid iron-sulfur protein (CoFeSP) is the primary methyl group donor and acceptor in biological carbon oxide conversion along the reductive acetyl-CoA pathway. Changes of the axial coordination of the cobalt ion within the corrin macrocycle upon redox transitions in aqua-, methyl-, and cyano-Cbl bound to CoFeSP or in solution were studied using X-ray absorption spectroscopy (XAS) at the Co K-edge in combination with density functional theory (DFT) calculations, supported by metal content and cobalt redox level quantification with further spectroscopic methods. Calculation of the highly variable pre-edge X-ray absorption features due to core-to-valence (ctv) electronic transitions, XANES shape analysis, and cobalt-ligand bond lengths determination from EXAFS has yielded models for the molecular and electronic structures of the cobalt sites. This suggested the absence of a ligand at cobalt in CoFeSP in α-position where the dimethylbenzimidazole (dmb) base of the cofactor is bound in Cbl in solution. As main species, (dmb)CoIII(OH2), (dmb)CoII(OH2), and (dmb)CoIII(CH3) sites for solution Cbl and CoIII(OH2), CoII(OH2), and CoIII(CH3) sites in CoFeSP-Cbl were identified. Our data support binding of a serine residue from the reductive-activator protein (RACo) of CoFeSP to the cobalt ion in the CoFeSP-RACo protein complex that stabilizes Co(II). The absence of an α-ligand at cobalt not only tunes the redox potential of the cobalamin cofactor into the physiological range, but is also important for CoFeSP reactivation.

show abstract

The extended reductive acetyl-CoA pathway: ATPases in metal cluster maturation and reductive activation

Cited by 18 publications

References 92 publications

Structural insight into metallocofactor maturation in carbon monoxide dehydrogenase

Structural insight into metallocofactor maturation in carbon monoxide dehydrogenase

Ligand binding at the A-cluster in full-length or truncated acetyl-CoA synthase studied by X-ray absorption spectroscopy

Axial Ligation and Redox Changes at the Cobalt Ion in Cobalamin Bound to Corrinoid Iron-Sulfur Protein (CoFeSP) or in Solution Characterized by XAS and DFT

Contact Info

Product

Resources

About