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EcoSal Plus

Domain 3:

Metabolism

Anaerobic Formate and Hydrogen Metabolism

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  • Authors: R. Gary Sawers1, Melanie Blokesch2, and August Böck3
  • Editor: Valley Stewart4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom; 2: Department of Biology I—Microbiology, University of Munich, Maria Ward Strasse 1a, 80638 Munich, Germany; 3: Department of Biology I—Microbiology, University of Munich, Maria Ward Strasse 1a, 80638 Munich, Germany; 4: University of California, Davis, Davis, CA
  • Received 10 March 2004 Accepted 17 June 2004 Published 09 September 2004
  • Address correspondence to August Böck august.boeck@lrz.uni-muenchen.de
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  • Abstract:

    During fermentative growth, degrades carbohydrates via the glycolytic route into two pyruvate molecules. Pyruvate can be reduced to lactate or nonoxidatively cleaved by pyruvate formate lyase into acetyl-coenzyme A (acetyl-CoA) and formate. Acetyl-CoA can be utilized for energy conservation in the phosphotransacetylase (PTA) and acetate kinase (ACK) reaction sequence or can serve as an acceptor for reducing equivalents gathered during pyruvate formation, through the action of alcohol dehydrogenase (AdhE). Formic acid is strongly acidic and has a redox potential of −420 mV under standard conditions and therefore can be classified as a high-energy compound. Its disproportionation into CO and molecular hydrogen (E −420 mV) via the formate hydrogenlyase (FHL) system is therefore of high selective value. The FHL reaction involves the participation of at least seven proteins, most of which are metalloenzymes, with requirements for iron, molybdenum, nickel, or selenium. Complex auxiliary systems incorporate these metals. Reutilization of the hydrogen evolved required the evolution of H oxidation systems, which couple the oxidation process to an appropriate energy-conserving terminal reductase. has two hydrogen-oxidizing enzyme systems. Finally, fermentation is the "last resort" of energy metabolism, since it gives the minimal energy yield when compared with respiratory processes. Consequently, fermentation is used only when external electron acceptors are absent. This has necessitated the establishment of regulatory cascades, which ensure that the metabolic capability is appropriately adjusted to the physiological condition. Here we review the genetics, biochemistry, and regulation of hydrogen metabolism and its hydrogenase maturation system.

  • Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4

Key Concept Ranking

Integral Membrane Proteins
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Chemicals
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Proteins
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Protein Transport
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Anaerobic Formate and Hydrogen Metabolism

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ecosalplus.3.5.4.citations
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/content/journal/ecosalplus/10.1128/ecosalplus.3.5.4
2004-09-09
2017-09-26

Abstract:

During fermentative growth, degrades carbohydrates via the glycolytic route into two pyruvate molecules. Pyruvate can be reduced to lactate or nonoxidatively cleaved by pyruvate formate lyase into acetyl-coenzyme A (acetyl-CoA) and formate. Acetyl-CoA can be utilized for energy conservation in the phosphotransacetylase (PTA) and acetate kinase (ACK) reaction sequence or can serve as an acceptor for reducing equivalents gathered during pyruvate formation, through the action of alcohol dehydrogenase (AdhE). Formic acid is strongly acidic and has a redox potential of −420 mV under standard conditions and therefore can be classified as a high-energy compound. Its disproportionation into CO and molecular hydrogen (E −420 mV) via the formate hydrogenlyase (FHL) system is therefore of high selective value. The FHL reaction involves the participation of at least seven proteins, most of which are metalloenzymes, with requirements for iron, molybdenum, nickel, or selenium. Complex auxiliary systems incorporate these metals. Reutilization of the hydrogen evolved required the evolution of H oxidation systems, which couple the oxidation process to an appropriate energy-conserving terminal reductase. has two hydrogen-oxidizing enzyme systems. Finally, fermentation is the "last resort" of energy metabolism, since it gives the minimal energy yield when compared with respiratory processes. Consequently, fermentation is used only when external electron acceptors are absent. This has necessitated the establishment of regulatory cascades, which ensure that the metabolic capability is appropriately adjusted to the physiological condition. Here we review the genetics, biochemistry, and regulation of hydrogen metabolism and its hydrogenase maturation system.

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Figures

Image of Figure 1
Figure 1

The bar represents the cytoplasmic membrane. The stoichiometry of each complex is unknown and, therefore, each component of the complex is represented only once. Components in each complex that have similar functions and exhibit amino acid sequence similarity share the same color. FDH-H and the Hyc components form FHL, the Hya gene products form Hyd-1, and the Hyb gene products form Hyd-2. It is anticipated that the Hyf enzyme complex will have an organization similar to FHL. Arrows show the putative path of electron flow through each complex.

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Image of Figure 2
Figure 2

(A) A simplified model of the FDH-H active site with the bound inhibitor nitrite is shown. The position of the molybdenum atom relative to the two MGD cofactors and amino acid residues arginine 333, histidine 141, and selenocysteine (U) 140 is shown. Details of the structure are presented in Boyington et al. ( 24 ). The coordinates for the structure were obtained from Protein Data Bank ID code 1fdi. (B) Scheme of the reaction mechanism proposed for FDH-H. The details of this mechanism are based on information presented in Boyington et al. ( 24 ) and Khangulov et al. ( 4 ). Hydrogen bonds are represented by dotted lines, and the dotted arrow indicates electron transfer between the molybdenum atom and the [4Fe-4S] cluster within the protein. X signifies the physiological electron acceptor. Oxidized benzyl viologen can function as an artificial electron acceptor in vitro.

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Image of Figure 3
Figure 3

Genes with products that share a similar function or that have similar amino acid sequences are the same color.

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Figure 4

See the text for details.

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Image of Figure 5
Figure 5

(A) Aerobic conditions. The dotted angled arrows with a cross indicate that no transcription occurs. The black dots signify formate. ⊕, positive effect on activity or gene expression; θ, negative effect. UAS, upstream activating sequence. (B) Fermentative conditions.

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Figure 6

The stoichiometry of the proteins within the complexes in vivo are not known. For details, see the text.

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Image of Figure 7
Figure 7

The proteins HypB, HypD, HypE, and HypF (shaded grey) participate in the maturation of all three hydrogenases. The proteins HypA and HypC and HybF and HybG are specific for hydrogenase 3 and hydrogenases 1 and 2, respectively. The maturation process is depicted by the numbers I to IV, corresponding to the maturation steps shown in Fig. 6 . For details, see the text.

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Tables

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Table 1

Comparison of the properties of the hydrogenase isoenzymes

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Table 2

Function of the fdhF and hyc operon gene products

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Table 3

Proposed function of the hyf operon gene products

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
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Table 4

Function of the gene products of the hya and hyb operons

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4
Generic image for table
Table 5

Characteristics of proteins involved in maturation of NiFe hydrogenases from

Citation: Sawers R, Blokesch M, Böck A. 2004. Anaerobic Formate and Hydrogen Metabolism, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.5.4

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