Escherichia coli pfs Transcription: Regulation and Proposed Roles in Autoinducer-2 Synthesis and Purine Excretion

Abstract

Pfs expression is required for several metabolic pathways and limits the production of autoinducer-2, a molecule proposed to play a central role in interspecies quorum sensing. The present study reveals physiological conditions and promoter DNA elements that regulate Escherichia coli pfs transcription. Pfs transcription is shown to rely on both sigma 70 and sigma 38 (rpoS), and the latter is subject to induction that increases pfs expression. Transcription is maximal as the cells approach stationary phase, and this level can be increased by salt stress through induction of sigma 38-dependent expression. The pfs promoter is shown to contain both positive and negative elements, which can be used by both forms of RNA polymerase. The negative element is contained within the overlapping dgt promoter, which is involved in purine metabolism. Consideration of the physiological roles of sigma 38 and dgt leads to a model for how autoinducer production is controlled under changing physiological conditions.The pfs gene, encoding the 5Ј-methylthioadenosine/S-adenosylhomocysteine nucleosidase enzyme, is required for polyamine synthesis, adenine and methionine salvage, removal of toxic metabolites, and creation of luxS-dependent autoinducers (AIs) of quorum sensing in Escherichia coli and related bacteria (5,22,26). As quorum sensing involves cell-to-cell signaling, it would be expected to be a highly regulated process. Gene fusions have shown that the pfs-luxS pathway of AI-2 synthesis is limited by the expression of pfs rather than luxS (3). Pfs expression rises as cells approach stationary phase and then falls. AI-2 synthesis follows a similar pattern (31). AI-2 is excreted until stationary phase is reached, when it begins to be imported (27,31). The sources of these regulatory events are not known, and their significance with respect to quorum sensing is not well understood. In interspecies quorum sensing, it has been proposed that products of the pfs/luxS pathway, AI-2 molecules, accumulate from multiple bacterial species and then signal the population to behave coordinately (12, 32). The issue is important because quorum sensing is a widespread phenomenon and has been invoked as a potential target of therapeutic intervention (2).Because the expression of pfs rises as stationary phase approaches (3), we considered the possibility that the source of the rise might be induction of rpoS-dependent transcription. rpoS encodes sigma 38, which is induced in response to multiple stresses and directs the transcription of numerous genes that deal with physiological stress (10). Its initial expression pattern mimics that seen for pfs; sigma 38 is induced as cells sense the stresses that will lead to the halt in growth that is characteristic of stationary phase (14). If sigma 38 were the source of pfs regulation, this would have implications for events such as quorum sensing, which is proposed to be controlled by the AI system.We now report that rpoS-dependent expression is indeed the source of pfs induction. Overall, pfs transcripti...

Growth Deficiencies of Neisseria meningitidis pfs and luxS Mutants Are Not Due to Inactivation of Quorum Sensing

“…In the same organisms, however, pfs is subject to environmental and growth phase-dependent regulation (2,14). Thus, it appears that expression profiles for pfs and luxS are organism specific.…”

Different aspects of bacterial communication signals

“…Two I-genes, pfs (in Salmonella enterica and E. coli), and luxS (in Vibrio spp. ), have been reported for the synthesis of AI-2 (Beeston et al Beeston and Surette 2002;Kim et al 2006). Homologs of LuxS for the synthesis of AI-2 have been found in over 30 Gram-positive and Gram-negative bacteria, such as Campylobacter jejuni, Helicobacter pylori, Clostridium perfringens, Bacillus subtilis, Staphylococcus aureus, Listeria innocua, Lactobacillus plantarum, Streptococcus pyogenes and Erwinia amylovora, but two types of receptor regulatory proteins are present; LuxP in Vibrio spp.…”

Methylthioadenosine/S‐adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism

“…Pfs is an integral component of the AI‐2 synthesis pathway. Indeed, AI‐2 production shows a tighter correlation with Pfs transcription than luxS gene expression in several bacteria including Salmonella enterica serovar typhimurium and Streptococcus suis (Beeston and Surette, 2002; Kim et al ., 2006; Han and Lu, 2009). In B. burgdorferi, luxS mutations affect transcription of several genes but this change in the transcriptome did not seem to affect transmission of bacteria through ticks or pathogenesis of the spirochaete in the mouse model of infection (Stevenson and Babb, 2002; Hubner et al ., 2003; Babb et al ., 2005).…”