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Molecular singularities in a pheromone sensor triumvirate desynchronize the competence-predation interplay in the human commensal Streptococcus salivarius

ABSTRACT: The human oral cavity is one of the most competing environments, considering the extent and diversity of the bacterial community that colonizes it, as well as the multiple stresses to which it is subjected. The commensal species Streptococcus salivarius is one of the first colonizers of the oral mucosa (tongue, gums, inner cheeks and tooth enamel) in infants and remains predominant throughout the life of an adult. In order to adapt to diverse and variable environmental conditions, S. salivarius triggers in a coordinated way two bacterial developmental processes: competence (acquisition of extracellular DNA and new genetic traits) and predation (secretion of cytotoxic molecule), via ComR, a transcription factor activatable by a "pheromone" peptide. Nevertheless, the activation of other transcriptional regulators can uncouple these 2 mechanisms to allow, for example, only the production of toxins without triggering the competence phase.

ORGANISM(S): Streptococcus salivarius

PROVIDER: GSE120640 | GEO | 2019/08/19

REPOSITORIES: GEO

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Project description:In bacteria, phenotypic heterogeneity rescues the need for diversity in isogenic populations and allow concomitant multiple survival strategies when choosing only one is too risky. This powerful tactic is exploited for competence in streptococci and results in a bimodal activation, where only a subset of the community triggers the system. Deciphering the mechanisms underlying this puzzling behavior has remained challenging, especially since its study has been mainly achieved in S. mutans, where two different but interconnected regulation networks control competence. In this work, we sought to determine the origin of bimodality associated to the ComRS system thanks to the simplified S. salivarius model that harbors no supplemental signaling system. Using a single cell fluorescence reporter system together with the overexpression of the main actors of the regulation network, we showed that the ComR intracellular concentration is directly linked to the proportion of competent cells in the population. We report that this type of activation requires a functional positive feedback loop acting on comS through Opp and a putative ComS exporter, PptAB. To determine the origin of the heterogeneity amplified by the loop, we developed a mathematical model suggesting that either noise on ComS or ComR abundance could explain bimodality. Because ComR abundance is central for competence bimodal activation, we conducted an in silico identification and a systematic deletion of all the Two Component Systems (TCS) present in S. salivarius and identified CovRS, a well described virulence regulator in GAS and GBS, as a repressor of comR transcription. In vitro direct binding of CovR with the promoter of comR and transcriptomics confirmed those data. As CovRS integrates environmental stimuli that control ComR intracellular concentration, it represents the missing puzzle piece bridging environmental conditions and competence (bimodal) activation in salivarius streptococci.

Project description:Bacterial competence is a genetically programmed process that is triggered as a response to environmental stimuli. DNA uptake from the extracellular milieu by competence requires the expression of a complex machinery composed of a competence pseudopilus and a DNA translocase. In L. pneumophila, it has been reported that microaerophilic conditions and genetic alteration of the competence repressors ComR and ProQ result in competence. We have analyzed the gene expression profiles of the proQ and comR mutants using the L. pneumophila Philadelphia-1 microarray. Many competence genes were found to be induced in the comR and proQ mutants and represent a defined, regulon. The gene expression profiling of the proQ and comR mutants was part of a study aimed at understanding the function of the processive 3'-5' exoribonuclease RNase R (rnr gene) in L. pneumophila. We found that the gene expression profile of the rnr mutant shares similarities with the gene expression profiles of the comR and proQ mutants and that loss of the exoribonuclease activity of RNase R was sufficient to induce competence development. RNase R is a processive 3'-5' exoribonuclease with a high degree of conservation in prokaryotes. Although some bacteria possess additional hydrolytic 3Â´-5-exoribonucleases such as RNase II, RNase R was found to be the only one predicted in the Legionella pneumophila genome. This provided a unique opportunity to study the role of RNase R in the absence of an additional RNase with similar enzymatic activity. We investigated the role of RNase R in the biology of Legionella pneumophila under various conditions and performed gene expression profiling using microarrays. At optimal growth temperature, loss of RNase R had no major consequence on bacterial growth and had a moderate impact on normal gene regulation. However, at lower temperatures loss of RNase R has a significant impact on bacterial growth and resulted in the accumulation of structured RNA degradation products. Concurrently, gene regulation was affected and specifically resulted in increased expression of the competence regulon. Loss of the exoribonuclease activity of RNase R was sufficient to induce competence development, a genetically-programmed process normally triggered as a response to environmental stimuli. Temperature-dependent expression of competence genes in the rnr mutant was found to be independent of the previously identified competence regulators comR and ProQ. comR: Three test samples and three reference samples were analyzed. The test sample being the strain KS79, a comR mutant of L. pneumophila strain JR32 which is used as a reference. proQ: Three test samples and three reference samples were analyzed. The test sample being the strain LELA3825, a proQ mutant of L. pneumophila strain JR32 which is used as a reference. rnr: Six test samples and six reference samples grown at 30Â°C or 37Â°C were analyzed. The test sample being the strain LELA559, a rnr mutant of L. pneumophila strain JR32 which is used as a reference.

Project description:Bacterial competence is a genetically programmed process that is triggered as a response to environmental stimuli. DNA uptake from the extracellular milieu by competence requires the expression of a complex machinery composed of a competence pseudopilus and a DNA translocase. In L. pneumophila, it has been reported that microaerophilic conditions and genetic alteration of the competence repressors ComR and ProQ result in competence. We have analyzed the gene expression profiles of the proQ and comR mutants using the L. pneumophila Philadelphia-1 microarray. Many competence genes were found to be induced in the comR and proQ mutants and represent a defined, regulon. The gene expression profiling of the proQ and comR mutants was part of a study aimed at understanding the function of the processive 3'-5' exoribonuclease RNase R (rnr gene) in L. pneumophila. We found that the gene expression profile of the rnr mutant shares similarities with the gene expression profiles of the comR and proQ mutants and that loss of the exoribonuclease activity of RNase R was sufficient to induce competence development. RNase R is a processive 3'-5' exoribonuclease with a high degree of conservation in prokaryotes. Although some bacteria possess additional hydrolytic 3´-5-exoribonucleases such as RNase II, RNase R was found to be the only one predicted in the Legionella pneumophila genome. This provided a unique opportunity to study the role of RNase R in the absence of an additional RNase with similar enzymatic activity. We investigated the role of RNase R in the biology of Legionella pneumophila under various conditions and performed gene expression profiling using microarrays. At optimal growth temperature, loss of RNase R had no major consequence on bacterial growth and had a moderate impact on normal gene regulation. However, at lower temperatures loss of RNase R has a significant impact on bacterial growth and resulted in the accumulation of structured RNA degradation products. Concurrently, gene regulation was affected and specifically resulted in increased expression of the competence regulon. Loss of the exoribonuclease activity of RNase R was sufficient to induce competence development, a genetically-programmed process normally triggered as a response to environmental stimuli. Temperature-dependent expression of competence genes in the rnr mutant was found to be independent of the previously identified competence regulators comR and ProQ.

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Molecular singularities in a pheromone sensor triumvirate desynchronize the competence-predation interplay in the human commensal Streptococcus salivarius

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