Abstract
In streptococci, entry in competence is dictated by ComX abundance. In Streptococcus thermophilus, production of ComX is transient and tightly regulated during growth: it is positively regulated by the cell-cell communication system ComRS during the activation phase and negatively regulated during the shut-off phase by unidentified late competence gene(s). Interestingly, most S. thermophilus strains are not or weakly transformable in permissive growth conditions (i.e., chemically defined medium, CDM), suggesting that some players of the ComRS regulatory pathway are limiting. Here, we combined mathematical modeling and experimental approaches to identify the components of the ComRS system which are critical for both dynamics and amplitude of ComX production in S. thermophilus. We built a deterministic, population-scaled model of the time-course regulation of specific ComX production in CDM growth conditions. Strains LMD-9 and LMG18311 were respectively selected as representative of highly and weakly transformable strains. Results from in silico simulations and in vivo luciferase activities show that ComR concentration is the main limiting factor for the level of comX expression and controls the kinetics of spontaneous competence induction in strain LMD-9. In addition, the model predicts that the poor transformability of strain LMG18311 results from a 10-fold lower comR expression level compared to strain LMD-9. In agreement, comR overexpression in both strains was shown to induce higher competence levels with deregulated kinetics patterns during growth. In conclusion, we propose that the level of ComR production is one important factor that could explain competence heterogeneity among S. thermophilus strains.
Highlights
Genetic plasticity is at the core of the adaptation and evolution strategies in bacteria
We hypothesized that the modeling of the ComRS regulatory pathway would recapitulate regulation of ComX production in those growth conditions
The LMD-9 strain of S. thermophilus was chosen as model strain since the competence regulating network of this strain has been extensively studied and a range of experimental data are available on the expression of key competence genes in wild type (WT) and competence-deficient backgrounds (Fontaine et al, 2010a, 2013; Gardan et al, 2013)
Summary
Genetic plasticity is at the core of the adaptation and evolution strategies in bacteria. Conjugation, transduction, and competence are the main HGT mechanisms, and define genetic exchange communities (Skippington and Ragan, 2011). Competence is defined as a transient physiological state that enables bacteria and archaea to take up exogenous naked DNA and to stably integrate it in their genome by homologous recombination (Johnsborg et al, 2007; Seitz and Blokesch, 2013). The transforming DNA can be passively or actively released from surrounding dead cells or siblings via a programmed cell lysis mechanism promoted by competent cells, respectively (Claverys et al, 2007; Berg et al, 2012; Wei and Havarstein, 2012; Borgeaud et al, 2015). Competence is increasingly viewed as a stress response that may increase adaptability and fitness in hostile conditions (Claverys et al, 2006; Perry et al, 2009; Charpentier et al, 2012; Dufour and Levesque, 2013)
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