Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria

ABSTRACT For free-living bacteria and archaea, the equivalent of the biological species concept does not exist, creating several obstacles to the study of the processes contributing to microbial diversification. These obstacles are particularly high in soil, where high bacterial diversity inhibits t...

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Autores principales:	Alexander B. Chase, Philip Arevalo, Eoin L. Brodie, Martin F. Polz, Ulas Karaoz, Jennifer B. H. Martiny
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Curtobacterium population structure gene flow microbial ecology ecotype Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/97947debf0d046a3aedea1975efc8381
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spelling	oai:doaj.org-article:97947debf0d046a3aedea1975efc83812021-11-15T15:59:41ZMaintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria10.1128/mBio.02361-192150-7511https://doaj.org/article/97947debf0d046a3aedea1975efc83812019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02361-19https://doaj.org/toc/2150-7511ABSTRACT For free-living bacteria and archaea, the equivalent of the biological species concept does not exist, creating several obstacles to the study of the processes contributing to microbial diversification. These obstacles are particularly high in soil, where high bacterial diversity inhibits the study of closely related genotypes and therefore the factors structuring microbial populations. Here, we isolated strains within a single Curtobacterium ecotype from surface soil (leaf litter) across a regional climate gradient and investigated the phylogenetic structure, recombination, and flexible gene content of this genomic diversity to infer patterns of gene flow. Our results indicate that microbial populations are delineated by gene flow discontinuities, with distinct populations cooccurring at multiple sites. Bacterial population structure was further delineated by genomic features allowing for the identification of candidate genes possibly contributing to local adaptation. These results suggest that the genetic structure within this bacterium is maintained both by ecological specialization in localized microenvironments (isolation by environment) and by dispersal limitation between geographic locations (isolation by distance). IMPORTANCE Due to the promiscuous exchange of genetic material and asexual reproduction, delineating microbial species (and, by extension, populations) remains challenging. Because of this, the vast majority of microbial studies assessing population structure often compare divergent strains from disparate environments under varied selective pressures. Here, we investigated the population structure within a single bacterial ecotype, a unit equivalent to a eukaryotic species, defined as highly clustered genotypic and phenotypic strains with the same ecological niche. Using a combination of genomic and computational analyses, we assessed the phylogenetic structure, extent of recombination, and flexible gene content of this genomic diversity to infer patterns of gene flow. To our knowledge, this study is the first to do so for a dominant soil bacterium. Our results indicate that bacterial soil populations, similarly to those in other environments, are structured by gene flow discontinuities and exhibit distributional patterns consistent with both isolation by distance and isolation by environment. Thus, both dispersal limitation and local environments contribute to the divergence among closely related soil bacteria as observed in macroorganisms.Alexander B. ChasePhilip ArevaloEoin L. BrodieMartin F. PolzUlas KaraozJennifer B. H. MartinyAmerican Society for MicrobiologyarticleCurtobacteriumpopulation structuregene flowmicrobial ecologyecotypeMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Curtobacterium population structure gene flow microbial ecology ecotype Microbiology QR1-502
spellingShingle	Curtobacterium population structure gene flow microbial ecology ecotype Microbiology QR1-502 Alexander B. Chase Philip Arevalo Eoin L. Brodie Martin F. Polz Ulas Karaoz Jennifer B. H. Martiny Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria
description	ABSTRACT For free-living bacteria and archaea, the equivalent of the biological species concept does not exist, creating several obstacles to the study of the processes contributing to microbial diversification. These obstacles are particularly high in soil, where high bacterial diversity inhibits the study of closely related genotypes and therefore the factors structuring microbial populations. Here, we isolated strains within a single Curtobacterium ecotype from surface soil (leaf litter) across a regional climate gradient and investigated the phylogenetic structure, recombination, and flexible gene content of this genomic diversity to infer patterns of gene flow. Our results indicate that microbial populations are delineated by gene flow discontinuities, with distinct populations cooccurring at multiple sites. Bacterial population structure was further delineated by genomic features allowing for the identification of candidate genes possibly contributing to local adaptation. These results suggest that the genetic structure within this bacterium is maintained both by ecological specialization in localized microenvironments (isolation by environment) and by dispersal limitation between geographic locations (isolation by distance). IMPORTANCE Due to the promiscuous exchange of genetic material and asexual reproduction, delineating microbial species (and, by extension, populations) remains challenging. Because of this, the vast majority of microbial studies assessing population structure often compare divergent strains from disparate environments under varied selective pressures. Here, we investigated the population structure within a single bacterial ecotype, a unit equivalent to a eukaryotic species, defined as highly clustered genotypic and phenotypic strains with the same ecological niche. Using a combination of genomic and computational analyses, we assessed the phylogenetic structure, extent of recombination, and flexible gene content of this genomic diversity to infer patterns of gene flow. To our knowledge, this study is the first to do so for a dominant soil bacterium. Our results indicate that bacterial soil populations, similarly to those in other environments, are structured by gene flow discontinuities and exhibit distributional patterns consistent with both isolation by distance and isolation by environment. Thus, both dispersal limitation and local environments contribute to the divergence among closely related soil bacteria as observed in macroorganisms.
format	article
author	Alexander B. Chase Philip Arevalo Eoin L. Brodie Martin F. Polz Ulas Karaoz Jennifer B. H. Martiny
author_facet	Alexander B. Chase Philip Arevalo Eoin L. Brodie Martin F. Polz Ulas Karaoz Jennifer B. H. Martiny
author_sort	Alexander B. Chase
title	Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria
title_short	Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria
title_full	Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria
title_fullStr	Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria
title_full_unstemmed	Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria
title_sort	maintenance of sympatric and allopatric populations in free-living terrestrial bacteria
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/97947debf0d046a3aedea1975efc8381
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Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria

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