Fumarate regulation of gene expression in Escherichia coli by the DcuSR (dcuSR genes) two-component regulatory system

Abstract

In Escherichia coli the genes encoding the anaerobic fumarate respiratory system are transcriptionally regulated by C4-dicarboxylates. The regulation is effected by a two-component regulatory system, DcuSR, consisting of a sensory histidine kinase (DcuS) and a response regulator (DcuR). DcuS and DcuR are encoded by the dcuSR genes (previously yjdHG) at 93.7 min on the calculated E. coli map. Inactivation of the dcuR and dcuS genes caused the loss of C4-dicarboxylate-stimulated synthesis of fumarate reductase (frdABCD genes) and of the anaerobic fumarate-succinate antiporter DcuB (dcuB gene). DcuS is predicted to contain a large periplasmic domain as the supposed site for C4-dicarboxylate sensing. Regulation by DcuR and DcuS responded to the presence of the C4-dicarboxylates fumarate, succinate, malate, aspartate, tartrate, and maleate. Since maleate is not taken up by the bacteria under these conditions, the carboxylates presumably act from without. Genes of the aerobic C4-dicarboxylate pathway encoding succinate dehydrogenase (sdhCDAB) and the aerobic succinate carrier (dctA) are only marginally or negatively regulated by the DcuSR system. The CitAB two-component regulatory system, which is highly similar to DcuSR, had no effect on C4-dicarboxylate regulation of any of the genes.

FIG. 1

Map positions and arrangement of the dcuSR (previously yjdHG) (A) and citAB (B) genes on the E. coli genome. The scale gives the DNA length in kilobases. The positions of the dcuSR and the citAB genes on the calculated E. coli map are shown. Data are from reference and the E. coli data bank.

FIG. 2

Overview of the suggested domain structure of the sensor kinase DcuS. The positions of characteristic sequence features and of the domains are indicated by the numbers. The transmembrane helices (TM) were predicted from the sequence. The Q linkers (Q) and the signature segments of the kinase domain (H, N, G1, F, and G2) (19) were identified by sequence alignments. For the segments, the positions of the naming amino acid residue are given (drawn according to reference 5).