Abstract

Streptococcus pneumoniae (pneumococcus) has remained a persistent cause of invasive and mucosal disease in humans despite the widespread use of antibiotics and vaccines. The resilience of this organism is due to its capacity for adaptation through the uptake and incorporation of new genetic material from the surrounding microbial community. DNA uptake and recombination is controlled by a tightly regulated quorum sensing system that is triggered by the extracellular accumulation of competence stimulating peptide (CSP). In this study, we demonstrate that CSP can stimulate the production of a diverse array of blp bacteriocins. This cross stimulation occurs through increased production and secretion of the bacteriocin pheromone, BlpC, and requires a functional competence regulatory system. We show that a highly conserved motif in the promoter of the operon encoding BlpC and its transporter mediates the upregulation by CSP. The accumulation of BlpC following CSP stimulation results in augmented activation of the entire blp locus. Using biofilm-grown organisms as a model for competition and genetic exchange on the mucosal surface, we demonstrate that DNA exchange is enhanced by bacteriocin secretion suggesting that co-stimulation of bacteriocins with competence provides an adaptive advantage. The blp and com regulatory pathways are believed to have diverged and specialized in a remote ancestor of pneumococcus. Despite this, the two systems have maintained a regulatory connection that promotes competition and adaptation by targeting for lysis a wide array of potential competitors while simultaneously providing the means for incorporation of their DNA.

Highlights

  • Streptococcus pneumoniae is an important human pathogen that resides primarily in the human nasopharynx

  • Coordinated Bacteriocin and Competence Expression in Pneumococcus triggered that result in the production of proteins required for DNA uptake and integration

  • We demonstrate that the secretion of small antimicrobial peptides called bacteriocins is induced during competence

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Summary

Introduction

Streptococcus pneumoniae (pneumococcus) is an important human pathogen that resides primarily in the human nasopharynx. The genome of pneumococcus is characterized by significant diversity that is a direct result of frequent genetic exchange with the surrounding microbial community including other pneumococci and related streptococcal species. This diversity results in changes in the capsule locus that allow for host-immune evasion and acquisition of antibiotic resistance genes that allow the organism to persist despite environmental pressures that favor elimination [1,2,3,4]. Many genes that encode the antagonistic fratricide effectors are upregulated during competence These proteins target non-competent cells in the population for lysis, presumably to provide a source of genetic material for DNA exchange [13,14,15,16]. This relatively limited repertoire of pherotypes makes cross induction of fratricide immunity between any two co-colonizing strains likely, potentially limiting DNA exchange [17,18,19]

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