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Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis

Bacillus subtilis is a soil bacterium that is competent for natural transformation. Genetically distinct B. subtilis swarms form a boundary upon encounter, resulting in killing of one of the strains. This process is mediated by a fast-evolving kin discrimination (KD) system consisting of cellular at...

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Autores principales: Stefanic, Polonca, Belcijan, Katarina, Kraigher, Barbara, Kostanjšek, Rok, Nesme, Joseph, Madsen, Jonas Stenløkke, Kovac, Jasna, Sørensen, Søren Johannes, Vos, Michiel, Mandic-Mulec, Ines
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8187645/
https://www.ncbi.nlm.nih.gov/pubmed/34103505
http://dx.doi.org/10.1038/s41467-021-23685-w
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author Stefanic, Polonca
Belcijan, Katarina
Kraigher, Barbara
Kostanjšek, Rok
Nesme, Joseph
Madsen, Jonas Stenløkke
Kovac, Jasna
Sørensen, Søren Johannes
Vos, Michiel
Mandic-Mulec, Ines
author_facet Stefanic, Polonca
Belcijan, Katarina
Kraigher, Barbara
Kostanjšek, Rok
Nesme, Joseph
Madsen, Jonas Stenløkke
Kovac, Jasna
Sørensen, Søren Johannes
Vos, Michiel
Mandic-Mulec, Ines
author_sort Stefanic, Polonca
collection PubMed
description Bacillus subtilis is a soil bacterium that is competent for natural transformation. Genetically distinct B. subtilis swarms form a boundary upon encounter, resulting in killing of one of the strains. This process is mediated by a fast-evolving kin discrimination (KD) system consisting of cellular attack and defence mechanisms. Here, we show that these swarm antagonisms promote transformation-mediated horizontal gene transfer between strains of low relatedness. Gene transfer between interacting non-kin strains is largely unidirectional, from killed cells of the donor strain to surviving cells of the recipient strain. It is associated with activation of a stress response mediated by sigma factor SigW in the donor cells, and induction of competence in the recipient strain. More closely related strains, which in theory would experience more efficient recombination due to increased sequence homology, do not upregulate transformation upon encounter. This result indicates that social interactions can override mechanistic barriers to horizontal gene transfer. We hypothesize that KD-mediated competence in response to the encounter of distinct neighbouring strains could maximize the probability of efficient incorporation of novel alleles and genes that have proved to function in a genomically and ecologically similar context.
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spelling pubmed-81876452021-07-01 Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis Stefanic, Polonca Belcijan, Katarina Kraigher, Barbara Kostanjšek, Rok Nesme, Joseph Madsen, Jonas Stenløkke Kovac, Jasna Sørensen, Søren Johannes Vos, Michiel Mandic-Mulec, Ines Nat Commun Article Bacillus subtilis is a soil bacterium that is competent for natural transformation. Genetically distinct B. subtilis swarms form a boundary upon encounter, resulting in killing of one of the strains. This process is mediated by a fast-evolving kin discrimination (KD) system consisting of cellular attack and defence mechanisms. Here, we show that these swarm antagonisms promote transformation-mediated horizontal gene transfer between strains of low relatedness. Gene transfer between interacting non-kin strains is largely unidirectional, from killed cells of the donor strain to surviving cells of the recipient strain. It is associated with activation of a stress response mediated by sigma factor SigW in the donor cells, and induction of competence in the recipient strain. More closely related strains, which in theory would experience more efficient recombination due to increased sequence homology, do not upregulate transformation upon encounter. This result indicates that social interactions can override mechanistic barriers to horizontal gene transfer. We hypothesize that KD-mediated competence in response to the encounter of distinct neighbouring strains could maximize the probability of efficient incorporation of novel alleles and genes that have proved to function in a genomically and ecologically similar context. Nature Publishing Group UK 2021-06-08 /pmc/articles/PMC8187645/ /pubmed/34103505 http://dx.doi.org/10.1038/s41467-021-23685-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Stefanic, Polonca
Belcijan, Katarina
Kraigher, Barbara
Kostanjšek, Rok
Nesme, Joseph
Madsen, Jonas Stenløkke
Kovac, Jasna
Sørensen, Søren Johannes
Vos, Michiel
Mandic-Mulec, Ines
Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis
title Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis
title_full Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis
title_fullStr Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis
title_full_unstemmed Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis
title_short Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis
title_sort kin discrimination promotes horizontal gene transfer between unrelated strains in bacillus subtilis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8187645/
https://www.ncbi.nlm.nih.gov/pubmed/34103505
http://dx.doi.org/10.1038/s41467-021-23685-w
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