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Metabolism

C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth

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  • Authors: Gottfried Unden1, and Alexandra Kleefeld
  • Editor: Valley Stewart2
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institut für Mikrobiologie und Weinforschung, Johannes Gutenberg-Universität, Becherweg 15, 55099 Mainz, Germany; 2: University of California, Davis, Davis, CA
  • Received 06 January 2004 Accepted 22 March 2004 Published 29 December 2004
  • Address correspondence to Gottfried Unden unden@uni-mainz.de
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  • Abstract:

    C-dicarboxylates, like succinate, fumarate, - and -malate, tartrate, and the C-dicarboxylic amino acid aspartate, support aerobic and anaerobic growth of and related bacteria and can serve as carbon and energy sources. In aerobic growth, the C-dicarboxylates are oxidized in the citric acid cycle. Due to the interruption of the citric acid cycle under anaerobic conditions, anaerobic metabolism of the C-dicarboxylates depends on fumarate reduction to succinate. In some related bacteria (e.g., ), degradation of C-dicarboxylates, like tartrate, uses a different mechanism and pathway. It requires the functioning of an Na-dependent and membrane-associated oxaloacetate decarboxylase. Due to the incomplete function of the citric acid cycle in anaerobic growth, succinate supports only aerobic growth of . This chapter describes the pathways of and differences in aerobic and anaerobic C-dicarboxylate metabolism and the physiological consequences. The citric acid cycle, fumarate respiration, and fumarate reductase are discussed here only in the context of aerobic and anaerobic C-dicarboxylate metabolism. Some recent aspects of C-dicarboxylate metabolism, such as transport and sensing of C-dicarboxylates, and their relationships are treated in more detail.

  • Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5

Key Concept Ranking

Fumarate Respiration
0.45377284
Nuclear Magnetic Resonance Spectroscopy
0.4124688
Bacterial Growth
0.36153308
Anaerobic Respiration
0.35840857
Fumarate Reductase
0.30055833
0.45377284

Article Version

An updated version has been published for this content:
C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth

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/content/journal/ecosalplus/10.1128/ecosalplus.3.4.5
2004-12-29
2017-11-21

Abstract:

C-dicarboxylates, like succinate, fumarate, - and -malate, tartrate, and the C-dicarboxylic amino acid aspartate, support aerobic and anaerobic growth of and related bacteria and can serve as carbon and energy sources. In aerobic growth, the C-dicarboxylates are oxidized in the citric acid cycle. Due to the interruption of the citric acid cycle under anaerobic conditions, anaerobic metabolism of the C-dicarboxylates depends on fumarate reduction to succinate. In some related bacteria (e.g., ), degradation of C-dicarboxylates, like tartrate, uses a different mechanism and pathway. It requires the functioning of an Na-dependent and membrane-associated oxaloacetate decarboxylase. Due to the incomplete function of the citric acid cycle in anaerobic growth, succinate supports only aerobic growth of . This chapter describes the pathways of and differences in aerobic and anaerobic C-dicarboxylate metabolism and the physiological consequences. The citric acid cycle, fumarate respiration, and fumarate reductase are discussed here only in the context of aerobic and anaerobic C-dicarboxylate metabolism. Some recent aspects of C-dicarboxylate metabolism, such as transport and sensing of C-dicarboxylates, and their relationships are treated in more detail.

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Figures

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Figure 1

The scheme gives the sequence of enzyme reactions for the degradation of succinate (Succ) in aerobic growth (1 succinate + 3.5 O → 4 CO + 7 HO). For simplicity, not all intermediates for the conversion of citrate to succinate, and of PEP to pyruvate (Pyr), are shown. AcCoA, acetyl-CoA; DctA, aerobic succinate uptake carrier; Sdh, succinate dehydrogenase SdhABCD; Fum, fumarase; Mal, malate; Mdh, cytosolic (NADH-dependent) malate dehydrogenase; Mqo, membrane-associated malate-quinone oxidoreductase; CS, citrate synthase; Mez, malic enzymes; OAA, oxaloacetic acid ; Pck, PEP carboxykinase; PDH, pyruvate dehydrogenase; TCA, tricarboxylic acid cycle. Membrane-associated enzymes are marked by their locations.

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Figure 2

The scheme shows the pathways for the uptake of C-dicarboxylates and their conversion to succinate by fumarate reduction. From the fumarate reductase system, only fumarate reductase is given; details of fumarate respiration are shown in Fig. 4 . DcuB, (anaerobic) C-dicarboxylate–succinate antiporter; DcuA, constitutive C-dicarboxylate carrier; AspA, aspartase; Mdh, malate dehydrogenase; FumB, (anaerobic) fumarase B; Frd, fumarate reductase; TtdT (or YgjE), putative tartrate-succinate antiporter; -Ttd, -tartrate dehydratase; Trt, tartrate; OAA, oxaloacetic acid.

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Figure 3

The scheme shows the major intermediates for the conversion of glucose to formate, acetate, and ethanol (mixed acid fermentation) and the reactions for the formation and excretion of succinate from PEP. Residual activities of the interrupted tricarboxylic acid (TCA) cycle are shaded with broken lines. Ac-CoA, acetyl-CoA; PTS, PEP-dependent phosphotransferase uptake for glucose; PFL, pyruvate formate lyase; Ppc, PEP carboxylase; FumB, (anaerobic) fumarase; FumC, (aerobic) fumarase; Frd, fumarate reductase; Mdh, NADH-dependent cytosolic malate dehydrogenase; Sdh, succinate dehydrogenase SdhABCD; DcuC, succinate export carrier; Pyr, pyruvate; OAA, oxaloacetic acid.

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Figure 4

The scheme gives the topology of the enzymes, including the sites for H release and consumption by the enzymes. For NADH-quinone reduction, a translocation of 2–4 H or Na/2 e is suggested. The reaction of fumarate reductase is not electrogenic. H-fumarate respiration yields a 2 H/fumarate ratio by a mechanism that depends on the orientation of the active sites for fumarate reduction and H oxidation. Fumarate reduction and H oxidation are coupled to the consumption or release, respectively, of 2 H in the cytoplasm and the periplasm. Whether hydrogenase 2 translocates protons by an additional mechanism is not known.

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Figure 5

The distances represent the differences in identical amino acid residues of the carriers or the corresponding putative gene products. Clustal W was used for the comparison (opening, end, extending, and separation gap penalties were 10, 10, 0.05, and 0.05, respectively). Abbreviations of strains: , ; , ; , ; , ; , ; , ; , ; , ; , ; , ; , ; , ; , ; , ; , ; , . Modified from reference 93 .

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Figure 6

In aerobic growth, DctA is the major carrier for uptake. In mutants, an unknown, presumably monocarboxylate carrier takes over the function of DctA at pH <6. DcuA presumably is inactive. In anaerobic growth, during growth by fumarate respiration, DcuB is the major carrier and catalyzes an electroneutral fumarate-succinate antiport. DcuB can be supported or replaced by DcuA. During glucose fermentation, succinate efflux is effected by DcuC, which can be supported by DcuB, DcuA, and other unknown efflux carriers. During anaerobic growth on tartrate, tartrate-succinate antiport is presumably catalyzed by the putative carrier TtdT (YgjE). The function of the gene product (DcuD) is unknown.

Modified from reference 93 .

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Figure 7

The scheme gives the genes and proteins (sensor, DcuS; response regulator, DcuR; antiporter, DcuB) of fumarate respiration as predicted from the protein sequences.

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Figure 8

The domain consists of four central β-sheets, which are surrounded by five α-helices ( 106 ). The N- and C-terminal helices of the periplasmic domain presumably are closely linked to transmembrane helices TM1 and TM2 of DcuS.

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Tables

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Table 1

Genes and proteins specific for C-dicarboxylate metabolism in

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5
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Table 2

Expression of genes of aerobic and anaerobic C-dicarboxylate metabolism of in response to electron acceptors (O, nitrate, and fumarate), glucose, and Fe

Citation: Unden G, Kleefeld A. 2004. C-Dicarboxylate Degradation in Aerobic and Anaerobic Growth, EcoSal Plus 2004; doi:10.1128/ecosalplus.3.4.5

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