Cargando…

Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity

DNA methylations play an important role in the biology of bacteria. Often associated with restriction modification (RM) systems, they are important drivers of bacterial evolution interfering in horizontal gene transfer events by providing a defence against foreign DNA invasion or by favouring geneti...

Descripción completa

Detalles Bibliográficos
Autores principales: Dordet-Frisoni, Emilie, Vandecasteele, Céline, Contarin, Rachel, Sagné, Eveline, Baranowski, Eric, Klopp, Christophe, Nouvel, Laurent-Xavier, Citti, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9465063/
https://www.ncbi.nlm.nih.gov/pubmed/35576144
http://dx.doi.org/10.1099/mgen.0.000829
_version_ 1784787708600647680
author Dordet-Frisoni, Emilie
Vandecasteele, Céline
Contarin, Rachel
Sagné, Eveline
Baranowski, Eric
Klopp, Christophe
Nouvel, Laurent-Xavier
Citti, Christine
author_facet Dordet-Frisoni, Emilie
Vandecasteele, Céline
Contarin, Rachel
Sagné, Eveline
Baranowski, Eric
Klopp, Christophe
Nouvel, Laurent-Xavier
Citti, Christine
author_sort Dordet-Frisoni, Emilie
collection PubMed
description DNA methylations play an important role in the biology of bacteria. Often associated with restriction modification (RM) systems, they are important drivers of bacterial evolution interfering in horizontal gene transfer events by providing a defence against foreign DNA invasion or by favouring genetic transfer through production of recombinogenic DNA ends. Little is known regarding the methylome of the Mycoplasma genus, which encompasses several pathogenic species with small genomes. Here, genome-wide detection of DNA methylations was conducted using single molecule real-time (SMRT) and bisulphite sequencing in several strains of Mycoplasma agalactiae , an important ruminant pathogen and a model organism. Combined with whole-genome analysis, this allowed the identification of 19 methylated motifs associated with three orphan methyltransferases (MTases) and eight RM systems. All systems had a homolog in at least one phylogenetically distinct Mycoplasma spp. Our study also revealed that several superimposed genetic events may participate in the M. agalactiae dynamic epigenomic landscape. These included (i) DNA shuffling and frameshift mutations that affect the MTase and restriction endonuclease content of a clonal population and (ii) gene duplication, erosion, and horizontal transfer that modulate MTase and RM repertoires of the species. Some of these systems were experimentally shown to play a major role in mycoplasma conjugative, horizontal DNA transfer. While the versatility of DNA methylation may contribute to regulating essential biological functions at cell and population levels, RM systems may be key in mycoplasma genome evolution and adaptation by controlling horizontal gene transfers.
format Online
Article
Text
id pubmed-9465063
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Microbiology Society
record_format MEDLINE/PubMed
spelling pubmed-94650632022-09-12 Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity Dordet-Frisoni, Emilie Vandecasteele, Céline Contarin, Rachel Sagné, Eveline Baranowski, Eric Klopp, Christophe Nouvel, Laurent-Xavier Citti, Christine Microb Genom Research Articles DNA methylations play an important role in the biology of bacteria. Often associated with restriction modification (RM) systems, they are important drivers of bacterial evolution interfering in horizontal gene transfer events by providing a defence against foreign DNA invasion or by favouring genetic transfer through production of recombinogenic DNA ends. Little is known regarding the methylome of the Mycoplasma genus, which encompasses several pathogenic species with small genomes. Here, genome-wide detection of DNA methylations was conducted using single molecule real-time (SMRT) and bisulphite sequencing in several strains of Mycoplasma agalactiae , an important ruminant pathogen and a model organism. Combined with whole-genome analysis, this allowed the identification of 19 methylated motifs associated with three orphan methyltransferases (MTases) and eight RM systems. All systems had a homolog in at least one phylogenetically distinct Mycoplasma spp. Our study also revealed that several superimposed genetic events may participate in the M. agalactiae dynamic epigenomic landscape. These included (i) DNA shuffling and frameshift mutations that affect the MTase and restriction endonuclease content of a clonal population and (ii) gene duplication, erosion, and horizontal transfer that modulate MTase and RM repertoires of the species. Some of these systems were experimentally shown to play a major role in mycoplasma conjugative, horizontal DNA transfer. While the versatility of DNA methylation may contribute to regulating essential biological functions at cell and population levels, RM systems may be key in mycoplasma genome evolution and adaptation by controlling horizontal gene transfers. Microbiology Society 2022-05-16 /pmc/articles/PMC9465063/ /pubmed/35576144 http://dx.doi.org/10.1099/mgen.0.000829 Text en © 2022 The Authors https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License.
spellingShingle Research Articles
Dordet-Frisoni, Emilie
Vandecasteele, Céline
Contarin, Rachel
Sagné, Eveline
Baranowski, Eric
Klopp, Christophe
Nouvel, Laurent-Xavier
Citti, Christine
Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity
title Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity
title_full Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity
title_fullStr Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity
title_full_unstemmed Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity
title_short Impacts of Mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity
title_sort impacts of mycoplasma agalactiae restriction-modification systems on pan-epigenome dynamics and genome plasticity
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9465063/
https://www.ncbi.nlm.nih.gov/pubmed/35576144
http://dx.doi.org/10.1099/mgen.0.000829
work_keys_str_mv AT dordetfrisoniemilie impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity
AT vandecasteeleceline impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity
AT contarinrachel impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity
AT sagneeveline impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity
AT baranowskieric impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity
AT kloppchristophe impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity
AT nouvellaurentxavier impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity
AT cittichristine impactsofmycoplasmaagalactiaerestrictionmodificationsystemsonpanepigenomedynamicsandgenomeplasticity