Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae.
A secreted competence-stimulating peptide (CSP), encoded by comC, constitutes, together with the two-component system ComD-ComE, the master switch for competence induction in Streptococcus pneumoniae. Interaction between CSP and its membrane-bound histidine-kinase receptor, ComD, is believed to lead to autophosphorylation of ComD, which then transphosphorylates the ComE response regulator to activate transcription of a limited set of genes, including the comCDE operon. This generates a positive feedback loop, amplifying the signal and co-ordinating competence throughout the population. On the other hand, the promoter(s) and proteins important for basal comCDE expression have not been defined. We now report that CSP-induced and basal comCDE transcription both initiate from the same promoter, P(E); that basal expression necessitates the presence of both ComD and a phosphate-accepting form of ComE, but not CSP; and that overexpression of ComE(R120S) triggers ComD-dependent transformation in the absence of CSP. These observations suggest that self-activation of ComD is required for basal comCDE expression. We also establish that transcriptional readthrough occurs across the tRNA(Arg5) terminator and contributes significantly to comCDE expression. Finally, we demonstrate by various means, including single-cell competence analysis with GFP, that readthrough is crucial to avoid the stochastic production of CSP non-responsive cells lacking ComD or ComE.
Martin
Bernard
B
Centre National de la Recherche Scientifique, LMGM-UMR5100, Toulouse, France.
Granadel
Chantal
C
Campo
Nathalie
N
Hénard
Vincent
V
Prudhomme
Marc
M
Claverys
Jean-Pierre
JP
D001426:Bacterial Proteins / Q000378:metabolism*; D004269:DNA, Bacterial / Q000378:metabolism; D015964:Gene Expression Regulation, Bacterial; D023061:Gene Order; D005798:Genes, Bacterial; D000071677:Histidine Kinase; D009876:Operon; D011401:Promoter Regions, Genetic; D011494:Protein Kinases / Q000378:metabolism*; D015398:Signal Transduction; D013296:Streptococcus pneumoniae / Q000235:genetics / Q000502:physiology*; D014158:Transcription, Genetic; D014169:Transformation, Bacterial
D001426:Bacterial Proteins; C103179:ComE protein, Streptococcus pneumoniae; D004269:DNA, Bacterial; C423628:competence factor, Streptococcus; D011494:Protein Kinases; D000071677:Histidine Kinase