Cargando…

Competence shut-off by intracellular pheromone degradation in salivarius streptococci

Competence for DNA transformation is a major strategy for bacterial adaptation and survival. Yet, this successful tactic is energy-consuming, shifts dramatically the metabolism, and transitory impairs the regular cell-cycle. In streptococci, complex regulatory pathways control competence deactivatio...

Descripción completa

Detalles Bibliográficos
Autores principales: Knoops, Adrien, Ledesma-García, Laura, Waegemans, Alexandra, Lamontagne, Morgane, Decat, Baptiste, Degand, Hervé, Morsomme, Pierre, Soumillion, Patrice, Delvigne, Frank, Hols, Pascal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9173638/
https://www.ncbi.nlm.nih.gov/pubmed/35613247
http://dx.doi.org/10.1371/journal.pgen.1010198
_version_ 1784722067465175040
author Knoops, Adrien
Ledesma-García, Laura
Waegemans, Alexandra
Lamontagne, Morgane
Decat, Baptiste
Degand, Hervé
Morsomme, Pierre
Soumillion, Patrice
Delvigne, Frank
Hols, Pascal
author_facet Knoops, Adrien
Ledesma-García, Laura
Waegemans, Alexandra
Lamontagne, Morgane
Decat, Baptiste
Degand, Hervé
Morsomme, Pierre
Soumillion, Patrice
Delvigne, Frank
Hols, Pascal
author_sort Knoops, Adrien
collection PubMed
description Competence for DNA transformation is a major strategy for bacterial adaptation and survival. Yet, this successful tactic is energy-consuming, shifts dramatically the metabolism, and transitory impairs the regular cell-cycle. In streptococci, complex regulatory pathways control competence deactivation to narrow its development to a sharp window of time, a process known as competence shut-off. Although characterized in streptococci whose competence is activated by the ComCDE signaling pathway, it remains unclear for those controlled by the ComRS system. In this work, we investigate competence shut-off in the major human gut commensal Streptococcus salivarius. Using a deterministic mathematical model of the ComRS system, we predicted a negative player under the control of the central regulator ComX as involved in ComS/XIP pheromone degradation through a negative feedback loop. The individual inactivation of peptidase genes belonging to the ComX regulon allowed the identification of PepF as an essential oligoendopeptidase in S. salivarius. By combining conditional mutants, transcriptional analyses, and biochemical characterization of pheromone degradation, we validated the reciprocal role of PepF and XIP in ComRS shut-off. Notably, engineering cleavage site residues generated ultra-resistant peptides producing high and long-lasting competence activation. Altogether, this study reveals a proteolytic shut-off mechanism of competence in the salivarius group and suggests that this mechanism could be shared by other ComRS-containing streptococci.
format Online
Article
Text
id pubmed-9173638
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-91736382022-06-08 Competence shut-off by intracellular pheromone degradation in salivarius streptococci Knoops, Adrien Ledesma-García, Laura Waegemans, Alexandra Lamontagne, Morgane Decat, Baptiste Degand, Hervé Morsomme, Pierre Soumillion, Patrice Delvigne, Frank Hols, Pascal PLoS Genet Research Article Competence for DNA transformation is a major strategy for bacterial adaptation and survival. Yet, this successful tactic is energy-consuming, shifts dramatically the metabolism, and transitory impairs the regular cell-cycle. In streptococci, complex regulatory pathways control competence deactivation to narrow its development to a sharp window of time, a process known as competence shut-off. Although characterized in streptococci whose competence is activated by the ComCDE signaling pathway, it remains unclear for those controlled by the ComRS system. In this work, we investigate competence shut-off in the major human gut commensal Streptococcus salivarius. Using a deterministic mathematical model of the ComRS system, we predicted a negative player under the control of the central regulator ComX as involved in ComS/XIP pheromone degradation through a negative feedback loop. The individual inactivation of peptidase genes belonging to the ComX regulon allowed the identification of PepF as an essential oligoendopeptidase in S. salivarius. By combining conditional mutants, transcriptional analyses, and biochemical characterization of pheromone degradation, we validated the reciprocal role of PepF and XIP in ComRS shut-off. Notably, engineering cleavage site residues generated ultra-resistant peptides producing high and long-lasting competence activation. Altogether, this study reveals a proteolytic shut-off mechanism of competence in the salivarius group and suggests that this mechanism could be shared by other ComRS-containing streptococci. Public Library of Science 2022-05-25 /pmc/articles/PMC9173638/ /pubmed/35613247 http://dx.doi.org/10.1371/journal.pgen.1010198 Text en © 2022 Knoops et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Knoops, Adrien
Ledesma-García, Laura
Waegemans, Alexandra
Lamontagne, Morgane
Decat, Baptiste
Degand, Hervé
Morsomme, Pierre
Soumillion, Patrice
Delvigne, Frank
Hols, Pascal
Competence shut-off by intracellular pheromone degradation in salivarius streptococci
title Competence shut-off by intracellular pheromone degradation in salivarius streptococci
title_full Competence shut-off by intracellular pheromone degradation in salivarius streptococci
title_fullStr Competence shut-off by intracellular pheromone degradation in salivarius streptococci
title_full_unstemmed Competence shut-off by intracellular pheromone degradation in salivarius streptococci
title_short Competence shut-off by intracellular pheromone degradation in salivarius streptococci
title_sort competence shut-off by intracellular pheromone degradation in salivarius streptococci
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9173638/
https://www.ncbi.nlm.nih.gov/pubmed/35613247
http://dx.doi.org/10.1371/journal.pgen.1010198
work_keys_str_mv AT knoopsadrien competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT ledesmagarcialaura competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT waegemansalexandra competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT lamontagnemorgane competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT decatbaptiste competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT degandherve competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT morsommepierre competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT soumillionpatrice competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT delvignefrank competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci
AT holspascal competenceshutoffbyintracellularpheromonedegradationinsalivariusstreptococci