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Intensive targeting of regulatory competence genes by transposable elements in streptococci

Abstract

Competence for natural transformation is a widespread developmental process of streptococci. By allowing the uptake and recombination of exogenous naked DNA into the genome, natural transformation, as transposable elements, plays a key role in the plasticity of bacterial genomes. We previously analysed the insertion sites of IS1548, an insertion sequence present in Streptococcus agalactiae and S. pyogenes, and showed that some targeted loci are involved in competence induction. In this work, we investigated on a large scale if loci coding for early competence factors (ComX and the two pheromone-dependent signalling systems ComCDE and ComRS) of streptococci are especially targeted by transposable elements. The transposable elements inserted in regions surrounding these genes and housekeeping genes used for Multilocus Sequence Typing (MLST) were systematically searched for. We found numerous insertion events in the close vicinity of early competence genes, but only very few into the MLST loci. The incidence of transposable elements, mainly insertion sequences, is particularly high in the intergenic regions surrounding comX alleles in numerous species belonging to most streptococcal groups. The identification of scarce disruptive insertions inside early competence genes indicates that the maintenance of competence is essential for streptococci. The specific association of transposable elements with intergenic regions bordering the main regulatory genes of competence may impact on the induction of transformability and so, on the genome plasticity and adaptive evolution of streptococci. This widespread phenomenon brings new perspectives on our understanding of competence regulation and its role in the bacterial life cycle.

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Acknowledgements

P. Siguier is thanked for her help during the submission of IS sequences to the ISfinder databank. Work in the teams of PH and BH was supported by the National Foundation for Scientific Research (FNRS) and the Research Department of the Communauté française de Belgique (Concerted Research Action). PH. is Senior Research Associate of the FNRS.

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Correspondence to Maud Fléchard or Philippe Gilot.

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Communicated by S. Hohmann.

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Fléchard, M., Lucchetti-Miganeh, C., Hallet, B. et al. Intensive targeting of regulatory competence genes by transposable elements in streptococci. Mol Genet Genomics 294, 531–548 (2019). https://doi.org/10.1007/s00438-018-1507-5

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Keywords

  • Natural transformation
  • Mobile genetic element
  • Insertion sequence
  • Streptococcus