Massive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics

ABSTRACT In this work, by comparing genomes of closely related individuals of Streptomyces isolated at a spatial microscale (millimeters or centimeters), we investigated the extent and impact of horizontal gene transfer in the diversification of a natural Streptomyces population. We show that despit...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Abdoul-Razak Tidjani, Jean-Noël Lorenzi, Maxime Toussaint, Erwin van Dijk, Delphine Naquin, Olivier Lespinet, Cyril Bontemps, Pierre Leblond
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://doaj.org/article/ff96284dea1648d4a50d21b447b6311a
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:ff96284dea1648d4a50d21b447b6311a
record_format dspace
spelling oai:doaj.org-article:ff96284dea1648d4a50d21b447b6311a2021-11-15T15:59:41ZMassive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics10.1128/mBio.01533-192150-7511https://doaj.org/article/ff96284dea1648d4a50d21b447b6311a2019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01533-19https://doaj.org/toc/2150-7511ABSTRACT In this work, by comparing genomes of closely related individuals of Streptomyces isolated at a spatial microscale (millimeters or centimeters), we investigated the extent and impact of horizontal gene transfer in the diversification of a natural Streptomyces population. We show that despite these conspecific strains sharing a recent common ancestor, all harbored significantly different gene contents, implying massive and rapid gene flux. The accessory genome of the strains was distributed across insertion/deletion events (indels) ranging from one to several hundreds of genes. Indels were preferentially located in the arms of the linear chromosomes (ca. 12 Mb) and appeared to form recombination hot spots. Some of them harbored biosynthetic gene clusters (BGCs) whose products confer an inhibitory capacity and may constitute public goods that can favor the cohesiveness of the bacterial population. Moreover, a significant proportion of these variable genes were either plasmid borne or harbored signatures of actinomycete integrative and conjugative elements (AICEs). We propose that conjugation is the main driver for the indel flux and diversity in Streptomyces populations. IMPORTANCE Horizontal gene transfer is a rapid and efficient way to diversify bacterial gene pools. Currently, little is known about this gene flux within natural soil populations. Using comparative genomics of Streptomyces strains belonging to the same species and isolated at microscale, we reveal frequent transfer of a significant fraction of the pangenome. We show that it occurs at a time scale enabling the population to diversify and to cope with its changing environment, notably, through the production of public goods.Abdoul-Razak TidjaniJean-Noël LorenziMaxime ToussaintErwin van DijkDelphine NaquinOlivier LespinetCyril BontempsPierre LeblondAmerican Society for MicrobiologyarticleStreptomycesconjugationgene transferplasticitypopulationMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution DOAJ
collection DOAJ
language EN
topic Streptomyces
conjugation
gene transfer
plasticity
population
Microbiology
QR1-502
spellingShingle Streptomyces
conjugation
gene transfer
plasticity
population
Microbiology
QR1-502
Abdoul-Razak Tidjani
Jean-Noël Lorenzi
Maxime Toussaint
Erwin van Dijk
Delphine Naquin
Olivier Lespinet
Cyril Bontemps
Pierre Leblond
Massive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics
description ABSTRACT In this work, by comparing genomes of closely related individuals of Streptomyces isolated at a spatial microscale (millimeters or centimeters), we investigated the extent and impact of horizontal gene transfer in the diversification of a natural Streptomyces population. We show that despite these conspecific strains sharing a recent common ancestor, all harbored significantly different gene contents, implying massive and rapid gene flux. The accessory genome of the strains was distributed across insertion/deletion events (indels) ranging from one to several hundreds of genes. Indels were preferentially located in the arms of the linear chromosomes (ca. 12 Mb) and appeared to form recombination hot spots. Some of them harbored biosynthetic gene clusters (BGCs) whose products confer an inhibitory capacity and may constitute public goods that can favor the cohesiveness of the bacterial population. Moreover, a significant proportion of these variable genes were either plasmid borne or harbored signatures of actinomycete integrative and conjugative elements (AICEs). We propose that conjugation is the main driver for the indel flux and diversity in Streptomyces populations. IMPORTANCE Horizontal gene transfer is a rapid and efficient way to diversify bacterial gene pools. Currently, little is known about this gene flux within natural soil populations. Using comparative genomics of Streptomyces strains belonging to the same species and isolated at microscale, we reveal frequent transfer of a significant fraction of the pangenome. We show that it occurs at a time scale enabling the population to diversify and to cope with its changing environment, notably, through the production of public goods.
format article
author Abdoul-Razak Tidjani
Jean-Noël Lorenzi
Maxime Toussaint
Erwin van Dijk
Delphine Naquin
Olivier Lespinet
Cyril Bontemps
Pierre Leblond
author_facet Abdoul-Razak Tidjani
Jean-Noël Lorenzi
Maxime Toussaint
Erwin van Dijk
Delphine Naquin
Olivier Lespinet
Cyril Bontemps
Pierre Leblond
author_sort Abdoul-Razak Tidjani
title Massive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics
title_short Massive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics
title_full Massive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics
title_fullStr Massive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics
title_full_unstemmed Massive Gene Flux Drives Genome Diversity between Sympatric <italic toggle="yes">Streptomyces</italic> Conspecifics
title_sort massive gene flux drives genome diversity between sympatric <italic toggle="yes">streptomyces</italic> conspecifics
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/ff96284dea1648d4a50d21b447b6311a
work_keys_str_mv AT abdoulrazaktidjani massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
AT jeannoellorenzi massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
AT maximetoussaint massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
AT erwinvandijk massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
AT delphinenaquin massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
AT olivierlespinet massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
AT cyrilbontemps massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
AT pierreleblond massivegenefluxdrivesgenomediversitybetweensympatricitalictoggleyesstreptomycesitalicconspecifics
_version_ 1718427007160680448