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J. Biol. Chem., Vol. 277, Issue 51, 49841-49849, December 20, 2002
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From the Department of Molecular Biology and Biotechnology, Krebs
Institute for Biomolecular Research, University of Sheffield, Firth
Court, Western Bank, Sheffield S10 2TN, United Kingdom
Assembly of Escherichia coli
cytochrome bd and periplasmic cytochromes requires the
ATP-binding cassette transporter CydDC, whose substrate is unknown.
Two-dimensional SDS-PAGE comparison of periplasm from wild-type and
cydD mutant strains revealed that the latter was deficient
in several periplasmic transport binding proteins, but no single major
protein was missing in the cydD periplasm. Instead, CydDC
exports from cytoplasm to periplasm the amino acid cysteine,
demonstrated using everted membrane vesicles that transported
radiolabeled cysteine inward in an ATP-dependent, uncoupler-independent manner. New pleiotropic cydD
phenotypes are reported, including sensitivity to benzylpenicillin and
dithiothreitol, and loss of motility, consistent with periplasmic
defects in disulfide bond formation. Exogenous cysteine reversed these
phenotypes and affected levels of periplasmic c-type
cytochromes in cydD and wild-type strains but did not
restore cytochrome d. Consistent with CydDC being a
cysteine exporter, cydD mutant growth was hypersensitive to
high cysteine concentrations and accumulated higher cytoplasmic cysteine levels, as did a mutant defective in
orf299, encoding a transporter of the major
facilitator superfamily. A cydD orf299 double mutant
was extremely cysteine-sensitive and had higher cytoplasmic cysteine
levels, whereas CydDC overexpression conferred resistance to high
extracellular cysteine concentrations. We propose that CydDC
exports cysteine, crucial for redox homeostasis in the periplasm.
Cysteine Is Exported from the Escherichia coli
Cytoplasm by CydDC, an ATP-binding Cassette-type Transporter Required
for Cytochrome Assembly*
*
This work was supported by Biotechnology and Biological
Sciences Research Council (BBSRC) Grant 50/P12980 (to R. K. P.) and a BBSRC research studentship (to H. C.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
To whom correspondence should be addressed. Tel.: 44-114-222-4447;
Fax: 44-114-272-8697; E-mail: r.poole@sheffield.ac.uk.
Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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