We report that the bgl operon of Escherichia coli, encoding the functions necessary for the uptake and metabolism of aryl--glucosides, is involved in the regulation of oligopeptide transport during stationary phase. Global analysis of intracellular proteins from Bgl-positive (Bgl ؉ ) and Bgl-negative (Bgl ؊ ) strains revealed that the operon exerts regulation on at least 12 downstream target genes. Of these, oppA, which encodes an oligopeptide transporter, was confirmed to be upregulated in the Bgl ؉ strain. Loss of oppA function results in a partial loss of the growth advantage in stationary-phase (GASP) phenotype of Bgl ؉ cells. The regulatory effect of the bgl operon on oppA expression is indirect and is mediated via gcvA, the activator of the glycine cleavage system, and gcvB, which regulates oppA at the posttranscriptional level. We show that BglG destabilizes the gcvA mRNA in vivo, leading to reduced expression of gcvA in the stationary phase. Deletion of gcvA results in the downregulation of gcvB and upregulation of oppA and can partially rescue the loss of the GASP phenotype seen in ⌬bglG strains. A possible mechanism by which oppA confers a competitive advantage to Bgl ؉ cells relative to Bgl ؊ cells is discussed.
In natural environments, bacteria live in close associations, most of the time under nutrient scarcity. This in turn leads to competition within populations for the limited resources that are available. Bacteria have evolved distinct mechanisms to extract utilizable substrates from available resources and consequently acquire a fitness advantage over competitors. One of the strategies is the exploitation of cryptic cellular functions encoded by genetic systems that are silent under laboratory conditions, such as the bgl (-glucoside) operon of Escherichia coli, involved in the uptake and metabolism of the plant-derived aromatic -glucosides salicin and arbutin (20).The three genes bglG, bglF, and bglB of the bgl operon are essential for the transport and hydrolysis of -glucosides (15, 27). The regulatory sequences involved in transcription initiation are located within the region bglR upstream of the structural genes. The product of bglG, the first gene of the operon, functions as an antiterminator at two rho-independent terminators flanking it (14,25). BglG is a sequence-specific RNA binding protein that interacts with a 37-nucleotide target sequence overlapping the terminator (10) known as the ribonucleic antiterminator (RAT) (3). The product of the second gene, BglF, is the bgl-specific component of the phosphotransferase system (PTS), which is also a negative regulator of the operon. BglF phosphorylates BglG in the absence of -glucosides, leading to its inactivation (1, 26). Thus, the BglG-BglF combination that mediates induction of the bgl operon in response to the presence of -glucosides resembles twocomponent signaling systems prevalent in bacteria. The third gene, bglB, encodes a phospho--glucosidase B that can hydrolyze the phosphorylated forms of salicin and arbutin.In spite of ...
