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Journal of Bacteriology, October 2000, p. 5757-5764, Vol. 182, No. 20
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Transport of C4-Dicarboxylates in Wolinella succinogenes

Roland Ullmann,1 Roland Gross,1 Jörg Simon,1 Gottfried Unden,2 and Achim Kröger1,*

Institut für Mikrobiologie, Johann Wolfgang Goethe-Universität, D-60439 Frankfurt am Main,1 and Institut für Mikrobiologie und Weinforschung, Johannes Gutenberg-Universität, D-55099 Mainz,2 Germany

Received 2 May 2000/Accepted 24 July 2000

C4-dicarboxylate transport is a prerequisite for anaerobic respiration with fumarate in Wolinella succinogenes, since the substrate site of fumarate reductase is oriented towards the cytoplasmic side of the membrane. W. succinogenes was found to transport C4-dicarboxylates (fumarate, succinate, malate, and aspartate) across the cytoplasmic membrane by antiport and uniport mechanisms. The electrogenic uniport resulted in dicarboxylate accumulation driven by anaerobic respiration. The molar ratio of internal to external dicarboxylate concentration was up to 103. The dicarboxylate antiport was either electrogenic or electroneutral. The electroneutral antiport required the presence of internal Na+, whereas the electrogenic antiport also operated in the absence of Na+. In the absence of Na+, no electrochemical proton potential (Delta p) was measured across the membrane of cells catalyzing fumarate respiration. This suggests that the proton potential generated by fumarate respiration is dissipated by the concomitant electrogenic dicarboxylate antiport. Three gene loci (dcuA, dcuB, and dctPQM) encoding putative C4-dicarboxylate transporters were identified on the genome of W. succinogenes. The predicted gene products of dcuA and dcuB are similar to the Dcu transporters that are involved in the fumarate respiration of Escherichia coli with external C4-dicarboxylates. The genes dctP, -Q, and -M probably encode a binding-protein-dependent secondary uptake transporter for dicarboxylates. A mutant (DcuA- DcuB-) of W. succinogenes lacking the intact dcuA and dcuB genes grew by nitrate respiration with succinate as the carbon source but did not grow by fumarate respiration with fumarate, malate, or aspartate as substrates. The DcuA-, DcuB-, and DctQM- mutants grew by fumarate respiration as well as by nitrate respiration with succinate as the carbon source. Cells of the DcuA- DcuB- mutant performed fumarate respiration without generating a proton potential even in the presence of Na+. This explains why the DcuA- DcuB- mutant does not grow by fumarate respiration. Growth by fumarate respiration appears to depend on the function of the Na+-dependent, electroneutral dicarboxylate antiport which is catalyzed exclusively by the Dcu transporters. Dicarboxylate transport via the electrogenic uniport is probably catalyzed by the DctPQM transporter and by a fourth, unknown transporter that may also operate as an electrogenic antiporter.

* Corresponding author. Mailing address: Institut für Mikrobiologie, Johann Wolfgang Goethe-Universität, Marie-Curie-Str. 9, D-60439 Frankfurt am Main, Germany. Phone: 49-69-79829507. Fax: 49-69-79829527. E-mail: A.Kroeger{at}em.uni-frankfurt.de.

Journal of Bacteriology, October 2000, p. 5757-5764, Vol. 182, No. 20
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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