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EcoSal Plus

Domain 3:

Metabolism

Anaerobic Formate and Hydrogen Metabolism

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  • Authors: Constanze Pinske1, and R. Gary Sawers2
  • Editor: Valley Stewart3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute of Biology/Microbiology, Martin Luther University, Halle-Wittenberg, 06120 Halle, Germany; 2: Institute of Biology/Microbiology, Martin Luther University Halle-Wittenberg, 06120 Halle, Germany; 3: University of California—Davis, Davis, CA
  • Received 14 June 2016 Accepted 20 July 2016 Published 04 October 2016
  • Address correspondence to Constanze Pinske, constanze.pinske@mikrobiologie.uni-halle.de; R. Gary Sawers, gary.sawers@mikrobiologie.uni-halle.de
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  • Abstract:

    Numerous recent developments in the biochemistry, molecular biology, and physiology of formate and H metabolism and of the [NiFe]-hydrogenase (Hyd) cofactor biosynthetic machinery are highlighted. Formate export and import by the aquaporin-like pentameric formate channel FocA is governed by interaction with pyruvate formate-lyase, the enzyme that generates formate. Formate is disproportionated by the reversible formate hydrogenlyase (FHL) complex, which has been isolated, allowing biochemical dissection of evolutionary parallels with complex I of the respiratory chain. A recently identified sulfido-ligand attached to Mo in the active site of formate dehydrogenases led to the proposal of a modified catalytic mechanism. Structural analysis of the homologous, H-oxidizing Hyd-1 and Hyd-5 identified a novel proximal [4Fe-3S] cluster in the small subunit involved in conferring oxygen tolerance to the enzymes. Synthesis of Typhimurium Hyd-5 occurs aerobically, which is novel for an enterobacterial Hyd. The O-sensitive Hyd-2 enzyme has been shown to be reversible: it presumably acts as a conformational proton pump in the H-oxidizing mode and is capable of coupling reverse electron transport to drive H release. The structural characterization of all the Hyp maturation proteins has given new impulse to studies on the biosynthesis of the Fe(CN)CO moiety of the [NiFe] cofactor. It is synthesized on a Hyp-scaffold complex, mainly comprising HypC and HypD, before insertion into the apo-large subunit. Finally, clear evidence now exists indicating that can mature Hyd enzymes differentially, depending on metal ion availability and the prevailing metabolic state. Notably, Hyd-3 of the FHL complex takes precedence over the H-oxidizing enzymes.

  • Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016

Key Concept Ranking

FhlA Transcriptional Activator
0.43863824
Integral Membrane Proteins
0.4224506
Dimethyl sulfoxide reductase
0.4102411
0.43863824

Article Version

This article is an updated version of the following content:

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0011-2016
2016-10-04
2017-07-21

Abstract:

Numerous recent developments in the biochemistry, molecular biology, and physiology of formate and H metabolism and of the [NiFe]-hydrogenase (Hyd) cofactor biosynthetic machinery are highlighted. Formate export and import by the aquaporin-like pentameric formate channel FocA is governed by interaction with pyruvate formate-lyase, the enzyme that generates formate. Formate is disproportionated by the reversible formate hydrogenlyase (FHL) complex, which has been isolated, allowing biochemical dissection of evolutionary parallels with complex I of the respiratory chain. A recently identified sulfido-ligand attached to Mo in the active site of formate dehydrogenases led to the proposal of a modified catalytic mechanism. Structural analysis of the homologous, H-oxidizing Hyd-1 and Hyd-5 identified a novel proximal [4Fe-3S] cluster in the small subunit involved in conferring oxygen tolerance to the enzymes. Synthesis of Typhimurium Hyd-5 occurs aerobically, which is novel for an enterobacterial Hyd. The O-sensitive Hyd-2 enzyme has been shown to be reversible: it presumably acts as a conformational proton pump in the H-oxidizing mode and is capable of coupling reverse electron transport to drive H release. The structural characterization of all the Hyp maturation proteins has given new impulse to studies on the biosynthesis of the Fe(CN)CO moiety of the [NiFe] cofactor. It is synthesized on a Hyp-scaffold complex, mainly comprising HypC and HypD, before insertion into the apo-large subunit. Finally, clear evidence now exists indicating that can mature Hyd enzymes differentially, depending on metal ion availability and the prevailing metabolic state. Notably, Hyd-3 of the FHL complex takes precedence over the H-oxidizing enzymes.

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Figures

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Figure 1

The curves are based on reference 299 . B, Representation of the main metabolic pathways competing for the degradation of formate under different conditions. See the text for details.

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Figure 2

A structure prediction was carried out for the Hyc (A) and Hyf (B and D) subunits and together with the structure of FDH-H, which is shown in blue (Protein Data Bank [PDB]: 1AA6), aligned to the complex I structure (PDB: 4HEA; C). The membrane proteins are shown in black and gray, the small subunits in dark green, and the HycF electron transfer subunit in light green. The [NiFe] active site in FHL is located in the purple HycE subunit, and the diaphorase NADH oxidation site is shown in red in complex I only. The oxidation site for FHL-2 is unknown, and a model showing the possible location according to FHL is shown in D.

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Figure 3

Genes whose products have a similar function or that have similar amino acid sequences are the same color, and a legend summarizes their function.

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Figure 4

A, The active site Mo-bis-PGD and the active site selenocysteine 140, His141, and Arg333 are shown. The red figure is based on PDB entry 2IV2 ( 71 ); the green figure is based on PDB entry 1AA6 ( 55 ). B, The proposed mechanism involves replacement of the SeCys ligand by formate, subsequent proton abstraction, possibly by the selenide, reduction of Mo to Mo during CO formation, and electron transfer to the [4Fe4S] cluster after which the proton is released. Here, the proton abstraction by selenide is shown, and alternative mechanisms are discussed in the text.

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Figure 5

The genes and distances are not to scale; the color scheme of genes is according to Fig. 3 . The gene product oligomerizes as a homotetramer and is able to sense formate under fermentative growth conditions, whereupon it activates transcription (green arrows). The binding site for activation is intergenic region 1 (IR1) and for is IR2. FHLA autoactivates its own transcription via the promoter; in the absence of formate, it is transcribed at a low constitutive level from its own promoter. The function of FHLA is antagonized by HycA, and by the small RNA OxyS, which binds to its mRNA, and the FHL complex removes the activating molecule formate (red arrows). Further transcriptional regulators to the respective promoters are shown in red (inhibiting) or green (activating).

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Figure 6

The horizontal gray bar represents the cytoplasmic membrane. Components in each complex that have similar functions and exhibit amino acid sequence similarity share the same color. Large subunits are shown in blue tones, small subunits in greens, and integral membrane subunits in gray. The metal cofactors are shown as spheres with FeS clusters in brown/yellow, the [NiFe] cofactor in green/brown, and the molybdopterin guanine dinucleotide is shown as spheres in FDH-H. The Hyd-1 structure is based on PDB entry 4GD3 with one heme molecule; an additional -type cytochrome subunit has been added as a cylinder. A structure prediction based on complex I is shown for FDH-H and the Hyc components that form the FHL complex. Dashed arrows show the putative path of electron flow through each complex. The lower part of the panel shows the products of the mixed acid fermentation, of which succinate is generated by reduction of fumarate by fumarate reductase (FRD) using electrons derived from the quinone pool. The formate generated is the substrate for the FHL complex, yielding H, which can be partially reoxidized by Hyd-1 and Hyd-2.

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Figure 7

For details, see the text. The inset shows the [NiFe] cofactor. The proteins are represented as structures (not to scale) and are modified from PDB files: 5AUO (HypAB), 2Z1C (HypC), 3VYR (HypCD), 3VYS + 3VYU + 3WJQ (HypCDE), 3VTI (HypEF), 2E85 (HycI), 3CGM (SlyD), while HycE and FHL are models.

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Figure 8

The carbamoyl phosphate synthetase (CarAB) phosphorylates hydrogen carbonate in an ATP-dependent reaction. Carbamoyl phosphate serves as the substrate for the ornithine carbamoyltransferases (ArgF/ArgI) during arginine biosynthesis. HypF competes for the use of carbamoyl phosphate in a hydrolysis reaction coupled to the formation of carbamoyl adenylate that can be transferred to HypE. Variations of these pathways are explained in the text. The carbon atom derived from hydrogen carbonate is highlighted in red.

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Tables

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Table 1

Comparison of the properties of the hydrogenase isoenzymes

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Table 2

Function and homology of and gene products

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Table 3

Function of the gene products of the and operons

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016
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Table 4

Proteins involved in maturation of [NiFe] hydrogenases from

Citation: Pinske C, Sawers R. 2016. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0011-2016

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