Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile

ABSTRACT Horizontal gene transfer (HGT) is a main driving force of bacterial evolution and innovation. This phenomenon was long thought to be marginal in mycoplasmas, a large group of self-replicating bacteria characterized by minute genomes as a result of successive gene losses during evolution. Re...

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Autores principales:	Emilie Dordet-Frisoni, Eveline Sagné, Eric Baranowski, Marc Breton, Laurent Xavier Nouvel, Alain Blanchard, Marc Serge Marenda, Florence Tardy, Pascal Sirand-Pugnet, Christine Citti
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/51db0264129b42e393d4f4a00d2cdc64
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spelling	oai:doaj.org-article:51db0264129b42e393d4f4a00d2cdc642021-11-15T15:47:04ZChromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile10.1128/mBio.01958-142150-7511https://doaj.org/article/51db0264129b42e393d4f4a00d2cdc642014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01958-14https://doaj.org/toc/2150-7511ABSTRACT Horizontal gene transfer (HGT) is a main driving force of bacterial evolution and innovation. This phenomenon was long thought to be marginal in mycoplasmas, a large group of self-replicating bacteria characterized by minute genomes as a result of successive gene losses during evolution. Recent comparative genomic analyses challenged this paradigm, but the occurrence of chromosomal exchanges had never been formally addressed in mycoplasmas. Here, we demonstrated the conjugal transfer of large chromosomal regions within and among ruminant mycoplasma species, with the incorporation of the incoming DNA occurring by homologous recombination into the recipient chromosome. By combining classical mating experiments with high-throughput next-generation sequencing, we documented the transfer of almost every position of the mycoplasma chromosome. Mycoplasma conjugation relies on the occurrence of an integrative conjugative element (ICE) in at least one parent cell. While ICE propagates horizontally from ICE-positive to ICE-negative cells, chromosomal transfers (CTs) occurred in the opposite direction, from ICE-negative to ICE-positive cells, independently of ICE movement. These findings challenged the classical mechanisms proposed for other bacteria in which conjugative CTs are driven by conjugative elements, bringing into the spotlight a new means for rapid mycoplasma innovation. Overall, they radically change our current views concerning the evolution of mycoplasmas, with particularly far-reaching implications given that over 50 species are human or animal pathogens. IMPORTANCE Horizontal gene transfers (HGT) shape bacterial genomes and are key contributors to microbial diversity and innovation. One main mechanism involves conjugation, a process that allows the simultaneous transfer of significant amounts of DNA upon cell-to-cell contact. Recognizing and deciphering conjugal mechanisms are thus essential in understanding the impact of gene flux on bacterial evolution. We addressed this issue in mycoplasmas, the smallest and simplest self-replicating bacteria. In these organisms, HGT was long thought to be marginal. We showed here that nearly every position of the Mycoplasma agalactiae chromosome could be transferred via conjugation, using an unconventional mechanism. The transfer involved DNA blocks containing up to 80 genes that were incorporated into the host chromosome by homologous recombination. These findings radically change our views concerning mycoplasma evolution and adaptation with particularly far-reaching implications given that over 50 species are human or animal pathogens.Emilie Dordet-FrisoniEveline SagnéEric BaranowskiMarc BretonLaurent Xavier NouvelAlain BlanchardMarc Serge MarendaFlorence TardyPascal Sirand-PugnetChristine CittiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Emilie Dordet-Frisoni Eveline Sagné Eric Baranowski Marc Breton Laurent Xavier Nouvel Alain Blanchard Marc Serge Marenda Florence Tardy Pascal Sirand-Pugnet Christine Citti Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile
description	ABSTRACT Horizontal gene transfer (HGT) is a main driving force of bacterial evolution and innovation. This phenomenon was long thought to be marginal in mycoplasmas, a large group of self-replicating bacteria characterized by minute genomes as a result of successive gene losses during evolution. Recent comparative genomic analyses challenged this paradigm, but the occurrence of chromosomal exchanges had never been formally addressed in mycoplasmas. Here, we demonstrated the conjugal transfer of large chromosomal regions within and among ruminant mycoplasma species, with the incorporation of the incoming DNA occurring by homologous recombination into the recipient chromosome. By combining classical mating experiments with high-throughput next-generation sequencing, we documented the transfer of almost every position of the mycoplasma chromosome. Mycoplasma conjugation relies on the occurrence of an integrative conjugative element (ICE) in at least one parent cell. While ICE propagates horizontally from ICE-positive to ICE-negative cells, chromosomal transfers (CTs) occurred in the opposite direction, from ICE-negative to ICE-positive cells, independently of ICE movement. These findings challenged the classical mechanisms proposed for other bacteria in which conjugative CTs are driven by conjugative elements, bringing into the spotlight a new means for rapid mycoplasma innovation. Overall, they radically change our current views concerning the evolution of mycoplasmas, with particularly far-reaching implications given that over 50 species are human or animal pathogens. IMPORTANCE Horizontal gene transfers (HGT) shape bacterial genomes and are key contributors to microbial diversity and innovation. One main mechanism involves conjugation, a process that allows the simultaneous transfer of significant amounts of DNA upon cell-to-cell contact. Recognizing and deciphering conjugal mechanisms are thus essential in understanding the impact of gene flux on bacterial evolution. We addressed this issue in mycoplasmas, the smallest and simplest self-replicating bacteria. In these organisms, HGT was long thought to be marginal. We showed here that nearly every position of the Mycoplasma agalactiae chromosome could be transferred via conjugation, using an unconventional mechanism. The transfer involved DNA blocks containing up to 80 genes that were incorporated into the host chromosome by homologous recombination. These findings radically change our views concerning mycoplasma evolution and adaptation with particularly far-reaching implications given that over 50 species are human or animal pathogens.
format	article
author	Emilie Dordet-Frisoni Eveline Sagné Eric Baranowski Marc Breton Laurent Xavier Nouvel Alain Blanchard Marc Serge Marenda Florence Tardy Pascal Sirand-Pugnet Christine Citti
author_facet	Emilie Dordet-Frisoni Eveline Sagné Eric Baranowski Marc Breton Laurent Xavier Nouvel Alain Blanchard Marc Serge Marenda Florence Tardy Pascal Sirand-Pugnet Christine Citti
author_sort	Emilie Dordet-Frisoni
title	Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile
title_short	Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile
title_full	Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile
title_fullStr	Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile
title_full_unstemmed	Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile
title_sort	chromosomal transfers in mycoplasmas: when minimal genomes go mobile
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/51db0264129b42e393d4f4a00d2cdc64
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Chromosomal Transfers in Mycoplasmas: When Minimal Genomes Go Mobile

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