Regulation of peptide transport in Escherichia coli: induction of the trp-linked operon encoding the oligopeptide permease

Abstract

Growth of Escherichia coli in medium containing leucine results in increased entry of exogenously supplied tripeptides into the bacterial cell. This leucine-mediated elevation of peptide transport required expression of the trp-linked opp operon and was accompanied by increased sensitivity to toxic tripeptides, by an enhanced capacity to utilize nutritional peptides, and by an increase in both the velocity and apparent steady-state level of L-[U-'4Cjalanyl-L-alanyl-L-alanine accumulation for E. coli grown in leucine-containing medium relative to these parameters of peptide transport measured with bacteria grown in media lacking leucine. Direct measurement of opp operon expression by pulse-labeling experiments demonstrated that growth of E. coli in the presence of leucine resulted in increased synthesis of the oppA-encoded periplasmic binding protein.Gram-negative bacteria such as Escherichia coli and Salmonella typhimurium utilize small oligopeptides as both carbon and nitrogen sources for growth. For these bacteria to grow on oligopeptides in the absence of periplasmic or extracellular peptidases (5, 18), the peptides must penetrate the permeability barriers posed by both the outer and cytoplasmic membranes. Data obtained with E. coli have shown that the composition of the outer membrane channels formed by the OmpF and OmpC porins imparts selectivity to the permeation of peptides through the outer membrane and that an E. coli outer membrane lacking both the ompF and the ompC gene products is peptide impermeable (1). Tripeptide passage through the second permeability barrier, the cytoplasmic membrane, requires the presence of specific, genetically defined transport systems. In E. coli tripeptide transport requires the protein products encoded by the genes of the trp-linked opp operon and the oppE locus (1, 12), whereas in S. typhimurium, tripeptide accumulation is mediated by uptake systems encoded by the opp operon and the tppB locus (6, 9). In both E. coli and S. typhimurium, the trp-linked opp operon is polycistronic with the first operon gene, oppA, encoding a periplasmic binding protein (1,7,8). The identity and function of the protein products of the other opp operon genes remain to be clearly defined. In contrast to the similarity found for the oligopeptide permease specified by the trp-linked opp operon of both E. coli and S. typhimurium, not only do the oppE locus of E. coli and the tppB locus of S. typhimurium appear, at present, to be genus specific, but also E. coli OppE-mutants and S. typhimurium TppB-mutants have unique tripeptide transport phenotypes. In E. coli, a mutation in oppE renders the strain resistant to certain toxic tripeptides and unable to utilize others as amino acid sources and influences the transport of tripeptides via the trp-linked system when the tripeptide substrate is present at low extracellular concentrations (1). The S. typhimurium tppB-encoded peptide transport system, on the other hand, lacks specificity with respect to the tripeptides that it will transport and appears ...

Relevance of Peptide Uptake Systems to the Physiology and Virulence of Streptococcus agalactiae

“…In several organisms, the expression of genes encoding peptide permeases is induced by the presence of peptides (7,25,44) or repressed in the absence of substrate (39,57). As shown by quantitative real-time PCR, the transcription of the S. agalactiae genes dppA to dppE was not affected in di-or hexapeptide-containing dCDM.…”

The leucine regulon of Escherichia coli K-12: a mutation in rblA alters expression of L-leucine-dependent metabolic operons

“…The presence of L-leucine during growth stimulated the wild-type activities five-and threefold, respectively, but had essentially no effect on the mutant levels ( (2,3). Leucine has been shown to stimulate transcription of this operon (2).…”

Specificity of peptide transport systems in Lactococcus lactis: evidence for a third system which transports hydrophobic di- and tripeptides

“…DtpP transport activity is higher when di-or tripeptides, i.e., substrates of the transport system, are present in the culture medium instead of amino acids or a complex nitrogen source. The regulation of peptide transport in bacteria has been addressed in a number of reports, and most transport systems appear to be regulated and expressed maximally when substrate is present (1,8). The role of Opp in the uptake of cell wall peptides in S. typhimurium provides an explanation for the constitutive expression of the oligopeptide permease, since cell wall peptide substrates need to be recycled under all conditions of growth (5,8).…”