Entry in competence state and subsequent extracellular DNA uptake generally provokes a concomitant secretion of antimicrobial peptides that burdens surrounding bacterial competitors and induces a DNA release originating from dead cells. In streptococci, the cell-cell communication module (ComCDE in S. pneumoniae or ComRS in S. mutans and S. thermophilus) controlling the production of the competence master regulator ComX also regulates BlpRH, a two-component system-based relay responsible for the production of bacteriocins (small ribosomally-encoded antibacterial peptides) production. Typically, the membrane-tethered BlpRH system directly activates all the genetic determinants of bacteriocin inhibitory effects, which are encoded in a major locus including genes of bacteriocin sensus stricto, associated immunity, and transport (blpAB). We report here a novel circuitry architecture in S. salivarius, a prevalent commensal inhabitant of the oral cavity. Although phylogenetically close to S. thermophilus, we observed in S. salivarius a decay in regulatory or transporter genes usually present within bacteriocin loci and a scattering of bacteriocin genes throughout the genome. Considering the gastro-intestinal tract colonizer strain HSISS4 that completely lost the BlpRH system, we highlighted with a combination of deep sequencing analyses, promoter probe assays and phenotypical tests that the ComS-activated ComR directly fires comX and all bacteriocin gene promoters to concomitantly induce competence and a multigenic predatory behaviour, bypassing the requirement for BlpRH orthologs. Furthermore, we showed that bacteriocins are secreted through ComA, a BlpAB paralog encoded in the comRS locus. Finally, we unearthed a ComR paralog that restores the uncoupling between competence and production of bacteriocins. Taken together, our results suggest that an evolutionary driving force in S. salivarius favours the loss of the Blp system at the profit of two pheromone-based cytoplasmic regulators that monopolize bacteriocin control.
Affiliations
UCLouvainSST/ISV - Institut des sciences de la vie
Mignolet, J., Hols, P., & et al. (2017). Ubiquitous rewiring of transcriptional control in streptococci: lesson from competence and predation coupling in Streptococcus salivarius. 12th Symposium on Lactic Acid Bacteria, Egmond aan Zzee. https://hdl.handle.net/2078.5/177263