Expression and maintenance of ComD–ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae

Authors

  • Bernard Martin,

    1. Centre National de la Recherche Scientifique, LMGM-UMR5100, F-31000 Toulouse, France.
    2. Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, F-31000 Toulouse, France.
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    • These authors contributed equally to this work.

  • Chantal Granadel,

    1. Centre National de la Recherche Scientifique, LMGM-UMR5100, F-31000 Toulouse, France.
    2. Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, F-31000 Toulouse, France.
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    • These authors contributed equally to this work.

  • Nathalie Campo,

    1. Centre National de la Recherche Scientifique, LMGM-UMR5100, F-31000 Toulouse, France.
    2. Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, F-31000 Toulouse, France.
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  • Vincent Hénard,

    1. Centre National de la Recherche Scientifique, LMGM-UMR5100, F-31000 Toulouse, France.
    2. Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, F-31000 Toulouse, France.
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  • Marc Prudhomme,

    1. Centre National de la Recherche Scientifique, LMGM-UMR5100, F-31000 Toulouse, France.
    2. Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, F-31000 Toulouse, France.
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  • Jean-Pierre Claverys

    Corresponding author
    1. Centre National de la Recherche Scientifique, LMGM-UMR5100, F-31000 Toulouse, France.
    2. Université de Toulouse, UPS, Laboratoire de Microbiologie et Génétique Moléculaires, F-31000 Toulouse, France.
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*E-mail claverys@ibcg.biotoul.fr; Tel. (+33) 561 33 59 11; Fax (+33) 561 33 58 86.

Summary

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, PE; that basal expression necessitates the presence of both ComD and a phosphate-accepting form of ComE, but not CSP; and that overexpression of ComER120S 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 tRNAArg5 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.

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