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Journal of Bacteriology, February 1999, p. 1238-1248, Vol. 181, No. 4
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Identification and Characterization of a
Two-Component Sensor-Kinase and Response-Regulator System
(DcuS-DcuR) Controlling Gene Expression in Response to
C4-Dicarboxylates in Escherichia
coli
Paul
Golby,1
Suzanne
Davies,2
David J.
Kelly,2
John R.
Guest,2 and
Simon C.
Andrews1,*
The School of Animal and Microbial Sciences,
University of Reading, Whiteknights, Reading RG6
6AJ,1 and
The Krebs Institute for
Biomolecular Research, Department of Molecular Biology and
Biotechnology, University of Sheffield, Western Bank, Sheffield S10
2TN,2 United Kingdom
Received 30 September 1998/Accepted 8 December 1998
The dcuB gene of Escherichia coli encodes
an anaerobic C4-dicarboxylate transporter that is induced
anaerobically by FNR, activated by the cyclic AMP receptor protein, and
repressed in the presence of nitrate by NarL. In addition,
dcuB expression is strongly induced by
C4-dicarboxylates, suggesting the presence of a novel
C4-dicarboxylate-responsive regulator in E. coli. This paper describes the isolation of a Tn10
mutant in which the 160-fold induction of dcuB expression
by C4-dicarboxylates is absent. The corresponding
Tn10 mutation resides in the yjdH gene, which
is adjacent to the yjdG gene and close to the
dcuB gene at ~93.5 min in the E. coli
chromosome. The yjdHG genes (redesignated
dcuSR) appear to constitute an operon encoding a
two-component sensor-regulator system (DcuS-DcuR). A plasmid carrying
the dcuSR operon restored the C4-dicarboxylate
inducibility of dcuB expression in the dcuS mutant to levels exceeding those of the dcuS+
strain by approximately 1.8-fold. The dcuS mutation
affected the expression of other genes with roles in
C4-dicarboxylate transport or metabolism. Expression of the
fumarate reductase (frdABCD) operon and the aerobic
C4-dicarboxylate transporter (dctA) gene were
induced 22- and 4-fold, respectively, by the DcuS-DcuR system in the
presence of C4-dicarboxylates. Surprisingly, anaerobic fumarate respiratory growth of the dcuS mutant was normal.
However, under aerobic conditions with C4-dicarboxylates as
sole carbon sources, the mutant exhibited a growth defect resembling
that of a dctA mutant. Studies employing a dcuA dcuB
dcuC triple mutant unable to transport
C4-dicarboxylates anaerobically revealed that C4-dicarboxylate transport is not required for
C4-dicarboxylate-responsive gene regulation. This suggests
that the DcuS-DcuR system responds to external substrates. Accordingly,
topology studies using 14 DcuS-BlaM fusions showed that DcuS contains
two putative transmembrane helices flanking a ~140-residue N-terminal
domain apparently located in the periplasm. This topology strongly
suggests that the periplasmic loop of DcuS serves as a
C4-dicarboxylate sensor. The cytosolic region of DcuS
(residues 203 to 543) contains two domains: a central PAS domain
possibly acting as a second sensory domain and a C-terminal transmitter
domain. Database searches showed that DcuS and DcuR are closely related
to a subgroup of two-component sensor-regulators that includes the
citrate-responsive CitA-CitB system of Klebsiella pneumoniae. DcuS is not closely related to the
C4-dicarboxylate-sensing DctS or DctB protein of
Rhodobacter capsulatus or rhizobial species, respectively.
Although all three proteins have similar topologies and functions, and
all are members of the two-component sensor-kinase family, their
periplasmic domains appear to have evolved independently.
*
Corresponding author. Mailing address: The School of
Animal and Microbial Sciences, University of Reading, Whiteknights, PO Box 228, Reading RG6 6AJ, United Kingdom. Phone: 118-987-5123, ext.
7045/7886. Fax: 118-931-0180. E-mail:
s.c.andrews{at}reading.ac.uk.
Journal of Bacteriology, February 1999, p. 1238-1248, Vol. 181, No. 4
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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