TY - JOUR

T1 - Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis

AU - Stefanic, Polonca

AU - Belcijan, Katarina

AU - Kraigher, Barbara

AU - Kostanjšek, Rok

AU - Nesme, Joseph

AU - Madsen, Jonas Stenløkke

AU - Kovac, Jasna

AU - Sørensen, Søren Johannes

AU - Vos, Michiel

AU - Mandic-Mulec, Ines

N1 - Funding Information: This work was supported by grants from Slovenian Research Agency (ARRS): the Programme Grant P4-0116, the Slovenia-USA collaboration grant bilateral ARRS project US/18-19-091 and ARRS projects: J4-9302, J4-8228, J4-7637 and the University infrastructural centre “Microscopy of biological samples” located in Biotechnical faculty, University of Ljubljana. Publisher Copyright: © 2021, The Author(s).

PY - 2021

Y1 - 2021

N2 - 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.

AB - 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.

U2 - 10.1038/s41467-021-23685-w

DO - 10.1038/s41467-021-23685-w

M3 - Journal article

C2 - 34103505

AN - SCOPUS:85107537620

VL - 12

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 3457

ER -