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Domain 3:

Metabolism

C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth

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  • Authors: Gottfried Unden1, Alexander Strecker2, Alexandra Kleefeld3, and Ok Bin Kim4
  • Editor: Valley Stewart5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute for Microbiology und Wine Research, Johannes Gutenberg-University, 55099 Mainz, Germany; 2: Institute for Microbiology und Wine Research, Johannes Gutenberg-University, 55099 Mainz, Germany; 3: Institute for Microbiology und Wine Research, Johannes Gutenberg-University, 55099 Mainz, Germany; 4: Department of Life Sciences, Ewha Womans University, 120-750 Seoul, Korea; 5: University of California—Davis, Davis, CA
  • Received 07 December 2015 Accepted 18 April 2016 Published 14 June 2016
  • Address correspondence to Gottfried Unden, unden@uni-mainz.de and Ok Bin Kim, kimokbin@ewha.ac.kr
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  • Abstract:

    C-dicarboxylates and the C-dicarboxylic amino acid -aspartate support aerobic and anaerobic growth of and related bacteria. In aerobic growth, succinate, fumarate, - and -malate, -aspartate, and -tartrate are metabolized by the citric acid cycle and associated reactions. Because of the interruption of the citric acid cycle under anaerobic conditions, anaerobic metabolism of C-dicarboxylates depends on fumarate reduction to succinate (fumarate respiration). In some related bacteria (e.g., ), utilization of C-dicarboxylates, such as tartrate, is independent of fumarate respiration and uses a Na-dependent membrane-bound oxaloacetate decarboxylase. Uptake of the C-dicarboxylates into the bacteria (and anaerobic export of succinate) is achieved under aerobic and anaerobic conditions by different sets of secondary transporters. Expression of the genes for C-dicarboxylate metabolism is induced in the presence of external C-dicarboxylates by the membrane-bound DcuS-DcuR two-component system. Noncommon C-dicarboxylates like -tartrate or -malate are perceived by cytoplasmic one-component sensors/transcriptional regulators. This article describes the pathways of aerobic and anaerobic C-dicarboxylate metabolism and their regulation. The citric acid cycle, fumarate respiration, and fumarate reductase are covered in other articles and discussed here only in the context of C-dicarboxylate metabolism. Recent aspects of C-dicarboxylate metabolism like transport, sensing, and regulation will be treated in more detail. This article is an updated version of an article published in 2004 in . The update includes new literature, but, in particular, the sections on the metabolism of noncommon C-dicarboxylates and their regulation, on the DcuS-DcuR regulatory system, and on succinate production by engineered are largely revised or new.

  • Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015

Key Concept Ranking

Fumarate Respiration
0.60191417
Acetyl Coenzyme A
0.49002934
Anaerobic Respiration
0.4289194
DmlR Transcriptional Regulator
0.4205918
0.60191417

Article Version

This article is an updated version of the following content:

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216. journal-id:
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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0021-2015
2016-06-14
2017-07-25

Abstract:

C-dicarboxylates and the C-dicarboxylic amino acid -aspartate support aerobic and anaerobic growth of and related bacteria. In aerobic growth, succinate, fumarate, - and -malate, -aspartate, and -tartrate are metabolized by the citric acid cycle and associated reactions. Because of the interruption of the citric acid cycle under anaerobic conditions, anaerobic metabolism of C-dicarboxylates depends on fumarate reduction to succinate (fumarate respiration). In some related bacteria (e.g., ), utilization of C-dicarboxylates, such as tartrate, is independent of fumarate respiration and uses a Na-dependent membrane-bound oxaloacetate decarboxylase. Uptake of the C-dicarboxylates into the bacteria (and anaerobic export of succinate) is achieved under aerobic and anaerobic conditions by different sets of secondary transporters. Expression of the genes for C-dicarboxylate metabolism is induced in the presence of external C-dicarboxylates by the membrane-bound DcuS-DcuR two-component system. Noncommon C-dicarboxylates like -tartrate or -malate are perceived by cytoplasmic one-component sensors/transcriptional regulators. This article describes the pathways of aerobic and anaerobic C-dicarboxylate metabolism and their regulation. The citric acid cycle, fumarate respiration, and fumarate reductase are covered in other articles and discussed here only in the context of C-dicarboxylate metabolism. Recent aspects of C-dicarboxylate metabolism like transport, sensing, and regulation will be treated in more detail. This article is an updated version of an article published in 2004 in . The update includes new literature, but, in particular, the sections on the metabolism of noncommon C-dicarboxylates and their regulation, on the DcuS-DcuR regulatory system, and on succinate production by engineered are largely revised or new.

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Figures

Image of Figure 1
Figure 1

Anaerobic utilization of -tartrate and citrate by and occurs by a different route that involves conversion of OAA (oxaloacetate) to pyruvate by a Na-dependent oxaloacetate decarboxylase (without fumarate respiration).

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Image of Figure 2
Figure 2

The scheme gives the sequence of enzyme reactions for the utilization of succinate (Succ) and other C-dicarboxylates in aerobic growth (1 succinate + 3.5 O→ 4 CO + 3 HO). For simplicity, not all intermediates for the conversion of citrate to succinate, and of PEP to pyruvate (Pyr), are shown. Membrane-associated or integral enzymes are indicated by their locations. DctA, SatP, and DauA are transporters for the uptake of the common C-dicarboxylates at pH > 6, pH 6, and pH 5, respectively. DctA catalyzes also the uptake of the noncommon C-dicarboxylates -malate and -tartrate under aerobic conditions. DcuA is produced constitutively and transports C-dicarboxylates and particularly -aspartate (-Asp). The pathway for aerobic oxidation of -tartrate is not known. AcCoA, acetyl-CoA; CS, citrate synthase; DctA, aerobic C-dicarboxylate transporter; DmlA, -malate dehydrogenase; Sdh, succinate dehydrogenase SdhABCD; FumA and FumC (aerobic) fumarase; Mal, malate; Mdh, cytosolic (NADH-dependent) malate dehydrogenase; Mqo, membrane-associated malate-quinone oxidoreductase; MaeB and SfcA, NAD(P)H-dependent malic enzymes; OAA, oxaloacetic acid; Pck, PEP carboxykinase; PDH, pyruvate dehydrogenase; TCA, tricarboxylic acid cycle. For details, see text.

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 3

(A) The scheme shows the pathways for the uptake of the C-dicarboxylates, conversion to fumarate, and formation of succinate by fumarate reduction. From the fumarate reductase system, only fumarate reductase is given; details of fumarate respiration are shown in Fig. 4 . DcuA is shown to function in -Asp/Succ antiport where -Asp utilization is linked to fumarate respiration (right part). (B) The scheme shows the role of DcuA in the constitutive uptake of -Asp (or other C-dicarboxylates) for anabolism (lower part), or in a hypothetical -Asp/Fum shuttle (upper part) where -Asp is supposed to serve as a source for ammonia only. AspA, aspartase; ET, electron transport; DcuA, constitutive C-dicarboxylate carrier; DcuB, (anaerobic) C-dicarboxylate/succinate antiporter; Frd, fumarate reductase; FumB, (anaerobic) fumarase B; MKH, menaquinol. See text for details.

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 4

The scheme gives the topology of the enzymes, including the sites for H release and consumption. For NADH-quinone reduction, a translocation of 4 H/2 e is suggested. The reaction of fumarate reductase is not electrogenic (H/2 e ratio of 0), whereas hydrogenase 2 is a redox-loop enzyme with a H/2 e ratio of 2. More details on fumarate respiration, see Unden et al. ( 60 ) and Tomasiek et al. ( 91 ).

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 5

DcuB, C-dicarboxylate/succinate antiporter; TtdT, -tartrate/succinate antiporter; TtdAB, tartrate dehydratase; Mdh, malate dehydrogenase; FumB, (anaerobic) fumarase B; Frd, fumarate reductase; ET, electron transport; MKH, menaquinol. Other details as described in Fig. 3 and in the text.

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 6

The figure gives stereoisomers of C-dicarboxylates carrying hydroxyl groups at C2, or at C2 and C3. Malate is found as -malate (2 configuration) and -malate (2 configuration), but only the -isomer is of natural origin. Tartrate is represented by three stereoisomers (-, - and -tartrate). -tartrate (2, 3 configuration) is present in many plants, whereas -tartrate (2, 3) is rare in nature and -tartrate not of natural origin. Fumarate and maleate are isomers of butenedioate. Maleate (-butenedioate) is chemically produced, whereas fumarate (-butenedioate) is a common intermediate of living cells.

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 7

(A) Synthesis of the citrate fermentation specific enzymes and transporters (CitT, citrate/succinate antiporter; CL, citrate lyase)is induced by CitA-CitB and citrate (blue labeling). Synthesis of the fumarate respiration pathway (FrdABCD [or Frd], FumB, presented in green) is induced by the citrate response of DcuS-DcuR (using the side-activity of DcuS for citrate). (B) This scheme, for comparison, gives the fumarate respiratory system (FrdABCD, Frd) and fumarate/succinate antiporter (DcuB) that are induced by DcuS-DcuR in response to fumarate (or C-dicarboxylates). The enzymes and the carrier shown in blue are unique for citrate fermentation; the enzymes shown in green are used both in citrate fermentation and fumarate respiration. Cit, citrate; Fum, fumarate; Mal, malate; OAA, oxaloacetate; Succ, succinate. Modified from reference 209 .

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 8

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

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 9

The scheme summarizes reactions engineered in to improve succinate production. Dotted arrows, either nonfunctional or decreased steps; Bold solid arrows, the primary route for carbon flow; Δ, gene deletion; +, overproduced or transformed genes; red letters, target genes; Ac-CoA, acetyl-CoA; Ace, acetate; Cit, citrate; DcuB, fumarate-succinate antiporter; DcuC, succinate export carrier; EMP, Embden-Meyerhof-Parnas pathway; EtOH, ethanol; For, formate; Fum, fumarate; GalP, galatose permease; G6P, glucose 6-phosphate; Isoc, isocitrate; Lac, lactate; Mal, malate; OAA, oxaloacetate; PEP, phosphoenolpyruvate; PTS, PEP-dependent phosphotransferase uptake for glucose; Pyr, pyruvate; Succ, succinate;. Genes: , isocitrate lyase; , malate synthase; , acetate kinase; , alcohol dehydrogenase; , anaerobic fumarase; , fumarate reductase; , glucokinase; , isocitrate lyase regulator; , lactate dehydrogenase; , NADH-dependent malate dehydrogenase; , pyruvate formate lyase; , pyruvate kinase; , PEP carboxylase; , PEP synthethase; , phosphate acetyl transferase.

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 10

The distances represent the differences in identical amino acid residues of the carriers or the corresponding gene products. The amino acid sequences were aligned with Clustal Omega program (http://www.ebi.ac.uk/Tools/msa/clustalo/) and the tree was reconstructed by the neighbor-joining method MEGA 6.0 ( 213 ). Abbreviations of strains: , ; , ; , ; , ; , ; , ; ; , ; , ; , ; ; Tk, ; , ; , .

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 11

(C) shows the transport modes for exchange, uptake, and efflux of C-dicarboxylates that can be effected by the Dcu carriers (DcuA, DcuB, or DcuC). Uptake and efflux are electrogenic by the symport of 3 H with the C-DC, whereas antiport is electroneutral ( 48 ). In aerobic growth (A), DctA is the major carrier for uptake at pH 7. DauA and potentially SatP replace DctA function at pH 5 and pH 6. The transporters catalyze electrogenic transport as presented in the figure. In anaerobic growth (B), 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 catalyzed by carrier TtdT. The function of the gene product (DcuD) is unknown. References and details in the text. Modified from reference 107 .

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 12

(A) DcuS is membrane-embedded by transmembrane helices 1 and 2 (TM1, TM2), and contains additionally the extracytoplasmic Per-Arndt-Sim domain PAS, a cytoplasmic PAS domain PAS, and a C-terminal HisKA/HATPase-type kinase. The monomers of the DcuS homodimer are presented in light and dark gray. In the dark gray monomer, the α-helical structure of TM2 and of the C-terminal helix α PAS is indicated. + and − indicate the periplasmic and cytoplasmic sides of the membrane. (B) Structure comparison of the periplasmic PAS domains of DcuS with -malate (brown; #3BY8 [ 93 ]) and CitA without citrate (gold, #2V9A). Structures were superimposed using the software Chimera ( 214 ). More details are given in ( 93 , 151 , 196 , 197 ). (C) For the DctA/DcuS complex, only monomers of the proteins are shown. DcuS is preferentially dimeric ( 195 ), whereas DctA is presumably a trimer ( 215 ). The C-terminal cytoplasmic helix 8b of DctA plays a central role in the interaction of DctA with DcuS ( 144 ). Helix 8b interacts with the PAS domain of DcuS and controls by the interaction the kinase activity of DcuS (see text for details).

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 13

B and C represent the functional state of DcuS in the DctA/DcuS sensor complex (C-dicarboxylate responsive DcuS). (A) shows DcuS without DctA (permanent active DcuS, constitutive ON). In the C-dicarboxylate responsive state (B, C), binding of C-dicarboxylates causes contraction of PAS with an uplift of α and of TM2 (red arrows) by one helical turn in TM2. The shift of TM2 is transmitted in the cytoplasm to PAS, causing relieved PAS dimerization and relief of kinase inhibition. DctA and PAS collaborate in silencing (or inhibiting) the activity of the kinase domain. PAS is only able to silence the kinase when properly positioned by DctA. DctA is therefore a cosilencer of PAS, and silencing of the kinase can be abolished artificially both by deletion of PAS or of DctA, or physiologically by the pulling of TM2 after C-dicarboxylate binding at PAS. See text for references.

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Figure 14

The common C-dicarboxylates and proteins/genes for general (central) C-dicarboxylate metabolism are presented in gray, proteins and genes of the noncommon C-dicarboxylate metabolism in orange. Dotted lines indicate that the type of regulation (direct or indirect) is not known. Arrow, induction; block, repression; common C-dicarboxylates, gray square; -malate, orange triangle; -tartrate, orange circles.

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Tables

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Table 1

Genes and proteins specific for C-dicarboxylate metabolism in

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015
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Table 2

Gene expression of enzymes for aerobic and anaerobic C-dicarboxylate metabolism of in response to electron acceptors (O, nitrate, and fumarate), carbon source, and other factors

Citation: Unden G, Strecker A, Kleefeld A, Kim O. 2016. C-Dicarboxylate Utilization in Aerobic and Anaerobic Growth, EcoSal Plus 2016; doi:10.1128/ecosalplus.ESP-0021-2015

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