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Gene flow and introgression are pervasive forces shaping the evolution of bacterial species

BACKGROUND: Although originally thought to evolve clonally, studies have revealed that most bacteria exchange DNA. However, it remains unclear to what extent gene flow shapes the evolution of bacterial genomes and maintains the cohesion of species. RESULTS: Here, we analyze the patterns of gene flow...

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Autores principales: Diop, Awa, Torrance, Ellis L., Stott, Caroline M., Bobay, Louis-Marie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650840/
https://www.ncbi.nlm.nih.gov/pubmed/36357919
http://dx.doi.org/10.1186/s13059-022-02809-5
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author Diop, Awa
Torrance, Ellis L.
Stott, Caroline M.
Bobay, Louis-Marie
author_facet Diop, Awa
Torrance, Ellis L.
Stott, Caroline M.
Bobay, Louis-Marie
author_sort Diop, Awa
collection PubMed
description BACKGROUND: Although originally thought to evolve clonally, studies have revealed that most bacteria exchange DNA. However, it remains unclear to what extent gene flow shapes the evolution of bacterial genomes and maintains the cohesion of species. RESULTS: Here, we analyze the patterns of gene flow within and between >2600 bacterial species. Our results show that fewer than 10% of bacterial species are truly clonal, indicating that purely asexual species are rare in nature. We further demonstrate that the taxonomic criterion of ~95% genome sequence identity routinely used to define bacterial species does not accurately represent a level of divergence that imposes an effective barrier to gene flow across bacterial species. Interruption of gene flow can occur at various sequence identities across lineages, generally from 90 to 98% genome identity. This likely explains why a ~95% genome sequence identity threshold has empirically been judged as a good approximation to define bacterial species. Our results support a universal mechanism where the availability of identical genomic DNA segments required to initiate homologous recombination is the primary determinant of gene flow and species boundaries in bacteria. We show that these barriers of gene flow remain porous since many distinct species maintain some level of gene flow, similar to introgression in sexual organisms. CONCLUSIONS: Overall, bacterial evolution and speciation are likely shaped by similar forces driving the evolution of sexual organisms. Our findings support a model where the interruption of gene flow—although not necessarily the initial cause of speciation—leads to the establishment of permanent and irreversible species borders. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02809-5.
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spelling pubmed-96508402022-11-15 Gene flow and introgression are pervasive forces shaping the evolution of bacterial species Diop, Awa Torrance, Ellis L. Stott, Caroline M. Bobay, Louis-Marie Genome Biol Research BACKGROUND: Although originally thought to evolve clonally, studies have revealed that most bacteria exchange DNA. However, it remains unclear to what extent gene flow shapes the evolution of bacterial genomes and maintains the cohesion of species. RESULTS: Here, we analyze the patterns of gene flow within and between >2600 bacterial species. Our results show that fewer than 10% of bacterial species are truly clonal, indicating that purely asexual species are rare in nature. We further demonstrate that the taxonomic criterion of ~95% genome sequence identity routinely used to define bacterial species does not accurately represent a level of divergence that imposes an effective barrier to gene flow across bacterial species. Interruption of gene flow can occur at various sequence identities across lineages, generally from 90 to 98% genome identity. This likely explains why a ~95% genome sequence identity threshold has empirically been judged as a good approximation to define bacterial species. Our results support a universal mechanism where the availability of identical genomic DNA segments required to initiate homologous recombination is the primary determinant of gene flow and species boundaries in bacteria. We show that these barriers of gene flow remain porous since many distinct species maintain some level of gene flow, similar to introgression in sexual organisms. CONCLUSIONS: Overall, bacterial evolution and speciation are likely shaped by similar forces driving the evolution of sexual organisms. Our findings support a model where the interruption of gene flow—although not necessarily the initial cause of speciation—leads to the establishment of permanent and irreversible species borders. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02809-5. BioMed Central 2022-11-10 /pmc/articles/PMC9650840/ /pubmed/36357919 http://dx.doi.org/10.1186/s13059-022-02809-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Diop, Awa
Torrance, Ellis L.
Stott, Caroline M.
Bobay, Louis-Marie
Gene flow and introgression are pervasive forces shaping the evolution of bacterial species
title Gene flow and introgression are pervasive forces shaping the evolution of bacterial species
title_full Gene flow and introgression are pervasive forces shaping the evolution of bacterial species
title_fullStr Gene flow and introgression are pervasive forces shaping the evolution of bacterial species
title_full_unstemmed Gene flow and introgression are pervasive forces shaping the evolution of bacterial species
title_short Gene flow and introgression are pervasive forces shaping the evolution of bacterial species
title_sort gene flow and introgression are pervasive forces shaping the evolution of bacterial species
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650840/
https://www.ncbi.nlm.nih.gov/pubmed/36357919
http://dx.doi.org/10.1186/s13059-022-02809-5
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