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Population genomics of early events in the ecological differentiation of bacteria.

ABSTRACT: Genetic exchange is common among bacteria, but its effect on population diversity during ecological differentiation remains controversial. A fundamental question is whether advantageous mutations lead to selection of clonal genomes or, as in sexual eukaryotes, sweep through populations on their own. Here, we show that in two recently diverged populations of ocean bacteria, ecological differentiation has occurred akin to a sexual mechanism: A few genome regions have swept through subpopulations in a habitat-specific manner, accompanied by gradual separation of gene pools as evidenced by increased habitat specificity of the most recent recombinations. These findings reconcile previous, seemingly contradictory empirical observations of the genetic structure of bacterial populations and point to a more unified process of differentiation in bacteria and sexual eukaryotes than previously thought.

SUBMITTER: Shapiro BJ

PROVIDER: S-EPMC3337212 | biostudies-literature | 2012 Apr

REPOSITORIES: biostudies-literature

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Population genomics of early events in the ecological differentiation of bacteria.

Shapiro B Jesse BJ Friedman Jonathan J Cordero Otto X OX Preheim Sarah P SP Timberlake Sonia C SC Szabó Gitta G Polz Martin F MF Polz Martin F MF Alm Eric J EJ

Science (New York, N.Y.) 20120401 6077

Genetic exchange is common among bacteria, but its effect on population diversity during ecological differentiation remains controversial. A fundamental question is whether advantageous mutations lead to selection of clonal genomes or, as in sexual eukaryotes, sweep through populations on their own. Here, we show that in two recently diverged populations of ocean bacteria, ecological differentiation has occurred akin to a sexual mechanism: A few genome regions have swept through subpopulations i ...[more]

PMID: 22491847

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Project description:Deciphering the genomic variation that represents microevolutionary processes toward species divergence is key to understanding microbial speciation, which has long been under debate. Streptomycetes are filamentous bacteria that are ubiquitous in nature and the richest source of antibiotics; however, their speciation processes remain unknown. To tackle this issue, we performed a comprehensive population genomics analysis on Streptomyces albidoflavus residing in different habitats and with a worldwide distribution and identified and characterized the foundational changes within the species. We detected three well-defined phylogenomic clades, of which clades I and III mainly contained free-living (soil/marine) and insect-associated strains, respectively, and clade II had a mixed origin. By performing genome-wide association studies (GWAS), we identified a number of genetic variants associated with free-living or entomic (denoting or relating to insects) habitats in both the accessory and core genomes. These variants contributed collectively to the population structure and had annotated or confirmed functions that likely facilitate differential adaptation of the species. In addition, we detected higher levels of homologous recombination within each clade and in the free-living group than within the whole species and in the entomic group. A subset of the insect-associated strains (clade III) showed a relatively independent evolutionary trajectory with more symbiosis-favorable genes but little genetic interchange with the other lineages. Our results demonstrate that ecological adaptation promotes genetic differentiation in S. albidoflavus, suggesting a model of ecological speciation with gene flow in streptomycetes.IMPORTANCE Species are the fundamental units of ecology and evolution, and speciation leads to the astounding diversity of life on Earth. Studying speciation is thus of great significance to understand, protect, and exploit biodiversity, but it is a challenge in the microbial world. In this study, using population genomics, we placed Streptomyces albidoflavus strains in a spectrum of speciation and showed that the genetic differences between phylogenomic clusters evolved mainly by environmental selection and gene-specific sweeps. These findings highlight the role of ecology in structuring recombining bacterial species, making a step toward a deeper understanding of microbial speciation. Our results also raise concerns of an underrated microbial diversity at the intraspecies level, which can be utilized for mining of ecologically relevant natural products.

Project description:Streptococcus mutans is widely recognized as one of the key etiological agents of human dental caries. Despite its role in this important disease, our present knowledge of gene content variability across the species and its relationship to adaptation is minimal. Estimates of its demographic history are not available. In this study, we generated genome sequences of 57 S. mutans isolates, as well as representative strains of the most closely related species to S. mutans (S. ratti, S. macaccae, and S. criceti), to identify the overall structure and potential adaptive features of the dispensable and core components of the genome. We also performed population genetic analyses on the core genome of the species aimed at understanding the demographic history, and impact of selection shaping its genetic variation. The maximum gene content divergence among strains was approximately 23%, with the majority of strains diverging by 5-15%. The core genome consisted of 1,490 genes and the pan-genome approximately 3,296. Maximum likelihood analysis of the synonymous site frequency spectrum (SFS) suggested that the S. mutans population started expanding exponentially approximately 10,000 years ago (95% confidence interval [CI]: 3,268-14,344 years ago), coincidental with the onset of human agriculture. Analysis of the replacement SFS indicated that a majority of these substitutions are under strong negative selection, and the remainder evolved neutrally. A set of 14 genes was identified as being under positive selection, most of which were involved in either sugar metabolism or acid tolerance. Analysis of the core genome suggested that among 73 genes present in all isolates of S. mutans but absent in other species of the mutans taxonomic group, the majority can be associated with metabolic processes that could have contributed to the successful adaptation of S. mutans to its new niche, the human mouth, and with the dietary changes that accompanied the origin of agriculture.

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Population genomics of early events in the ecological differentiation of bacteria.

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Population genomics of early events in the ecological differentiation of bacteria.

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