Eavesdropping and crosstalk between secreted quorum sensing peptide signals that regulate bacteriocin production in Streptococcus pneumoniae

Abstract

Quorum sensing (QS), where bacteria secrete and respond to chemical signals to coordinate population-wide behaviors, has revealed that bacteria are highly social. Here, we investigate how diversity in QS signals and receptors can modify social interactions controlled by the QS system regulating bacteriocin secretion in Streptococcus pneumoniae, encoded by the blp operon (bacteriocin-like peptide). Analysis of 4 096 pneumococcal genomes detected nine blp QS signals (BlpC) and five QS receptor groups (BlpH). Imperfect concordance between signals and receptors suggested widespread social interactions between cells, specifically eavesdropping (where cells respond to signals that they do not produce) and crosstalk (where cells produce signals that non-clones detect). This was confirmed in vitro by measuring the response of reporter strains containing six different blp QS receptors to cognate and non-cognate peptides. Assays between pneumococcal colonies grown adjacent to one another provided further evidence that crosstalk and eavesdropping occur at endogenous levels of signal secretion. Finally, simulations of QS strains producing bacteriocins revealed that eavesdropping can be evolutionarily beneficial even when the affinity for non-cognate signals is very weak. Our results highlight that social interactions can mediate intraspecific competition among bacteria and reveal that competitive interactions can be modified by polymorphic QS systems.

Bacterial antagonism in host-associated microbial communities

“…Some bacteria, including L. gasseri EV1461, can "eavesdrop" on the quorum-sensing signals of competing species and respond by expressing broad-spectrum antibiotics, as well as by generating antimicrobial resistance strategies (42,89,92,93). Notably, the blp quorum-sensing system that regulates bacteriocin production in S. pneumoniae is highly polymorphic, and instances of cross-talk and eavesdropping between strains are common (9). Simulations using four strains with varying ability to sense neighbor's quorum-sensing signals show that eavesdropping can confer a fitness advantage with a negative frequency dependence (a strain present at low frequency can induce bacteriocin production to invade a more abundant population).…”

“…Many toxins only target strains of the same species and therefore may not affect other competitors in the community. Further, the synthesis and secretion of these toxins may be physiologically costly and thus affect fitness (8,9). Toxins whose release requires cell lysis can only be deployed by a fraction of the population and will have different relative fitness costs and dynamics compared with actively secreted toxins.…”

Bacterial Community Interactions During Chronic Respiratory Disease

“…Cell to cell communication is an essential component of bacterial communities in order to modulate gene expression to best ensure survival. Although quorum sensing (QS) and interspecies communication can be used cooperatively in microbial communities, this pathway can also be exploited, allowing species to "eavesdrop" on neighboring species (Miller et al, 2018). QS can be blocked by inhibiting the production of signal, delivery of the signal, or detection of the signal.…”

Challenges and Limitations of Anti-quorum Sensing Therapies

“…Signaling associated with AI-2 in these bacteria is associated with adaptation to environmental conditions, affecting biofilm formation (Rickard et al, 2006; Lebeer et al, 2007; Cuadra-Saenz et al, 2012; Sun et al, 2014; Liu et al, 2017, 2018a) and resistance to stressors during the passage through the digestive tract (Yeo et al, 2015; Liu et al, 2018a). Additionally, the luxS system is required for the synthesis of bacteriocins by Escherichia coli (Lu et al, 2017), Streptococcus pneumoniae (Miller et al, 2018), Streptococcus mutans (Merritt et al, 2005; Sztajer et al, 2008), and Lactobacillus (Jia et al, 2017; Li et al, 2019). It was observed that AI-2 produced by Aggregatibacter actinomycetemcomitans is a factor directly involved in the inhibition of both biofilm formation and transformation into the filamentous form by Candida albicans (Bachtiar et al, 2014).…”