Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.

Horizontal gene transfer (HGT) is recognized as the major force for bacterial genome evolution. Yet, numerous questions remain about the transferred genes, their function, quantity and frequency. The extent to which genetic transformation by exogenous DNA has occurred over evolutionary time was init...

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Main Authors: Saliou Fall, Anne Mercier, Franck Bertolla, Alexandra Calteau, Laurent Gueguen, Guy Perrière, Timothy M Vogel, Pascal Simonet
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-10-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0001055
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author Saliou Fall
Anne Mercier
Franck Bertolla
Alexandra Calteau
Laurent Gueguen
Guy Perrière
Timothy M Vogel
Pascal Simonet
author_facet Saliou Fall
Anne Mercier
Franck Bertolla
Alexandra Calteau
Laurent Gueguen
Guy Perrière
Timothy M Vogel
Pascal Simonet
author_sort Saliou Fall
collection DOAJ
description Horizontal gene transfer (HGT) is recognized as the major force for bacterial genome evolution. Yet, numerous questions remain about the transferred genes, their function, quantity and frequency. The extent to which genetic transformation by exogenous DNA has occurred over evolutionary time was initially addressed by an in silico approach using the complete genome sequence of the Ralstonia solanacearum GMI1000 strain. Methods based on phylogenetic reconstruction of prokaryote homologous genes families detected 151 genes (13.3%) of foreign origin in the R. solanacearum genome and tentatively identified their bacterial origin. These putative transfers were analyzed in comparison to experimental transformation tests involving 18 different genomic DNA positions in the genome as sites for homologous or homeologous recombination. Significant transformation frequency differences were observed among these positions tested regardless of the overall genomic divergence of the R. solanacearum strains tested as recipients. The genomic positions containing the putative exogenous DNA were not systematically transformed at the highest frequencies. The two genomic "hot spots", which contain recA and mutS genes, exhibited transformation frequencies from 2 to more than 4 orders of magnitude higher than positions associated with other genes depending on the recipient strain. These results support the notion that the bacterial cell is equipped with active mechanisms to modulate acquisition of new DNA in different genomic positions. Bio-informatics study correlated recombination "hot-spots" to the presence of Chi-like signature sequences with which recombination might be preferentially initiated. The fundamental role of HGT is certainly not limited to the critical impact that the very rare foreign genes acquired mainly by chance can have on the bacterial adaptation potential. The frequency to which HGT with homologous and homeologous DNA happens in the environment might have led the bacteria to hijack DNA repair mechanisms in order to generate genetic diversity without losing too much genomic stability.
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spelling doaj.art-b07bf60064b3468d98b06f7e11a2e9902022-12-21T23:14:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032007-10-01210e105510.1371/journal.pone.0001055Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.Saliou FallAnne MercierFranck BertollaAlexandra CalteauLaurent GueguenGuy PerrièreTimothy M VogelPascal SimonetHorizontal gene transfer (HGT) is recognized as the major force for bacterial genome evolution. Yet, numerous questions remain about the transferred genes, their function, quantity and frequency. The extent to which genetic transformation by exogenous DNA has occurred over evolutionary time was initially addressed by an in silico approach using the complete genome sequence of the Ralstonia solanacearum GMI1000 strain. Methods based on phylogenetic reconstruction of prokaryote homologous genes families detected 151 genes (13.3%) of foreign origin in the R. solanacearum genome and tentatively identified their bacterial origin. These putative transfers were analyzed in comparison to experimental transformation tests involving 18 different genomic DNA positions in the genome as sites for homologous or homeologous recombination. Significant transformation frequency differences were observed among these positions tested regardless of the overall genomic divergence of the R. solanacearum strains tested as recipients. The genomic positions containing the putative exogenous DNA were not systematically transformed at the highest frequencies. The two genomic "hot spots", which contain recA and mutS genes, exhibited transformation frequencies from 2 to more than 4 orders of magnitude higher than positions associated with other genes depending on the recipient strain. These results support the notion that the bacterial cell is equipped with active mechanisms to modulate acquisition of new DNA in different genomic positions. Bio-informatics study correlated recombination "hot-spots" to the presence of Chi-like signature sequences with which recombination might be preferentially initiated. The fundamental role of HGT is certainly not limited to the critical impact that the very rare foreign genes acquired mainly by chance can have on the bacterial adaptation potential. The frequency to which HGT with homologous and homeologous DNA happens in the environment might have led the bacteria to hijack DNA repair mechanisms in order to generate genetic diversity without losing too much genomic stability.https://doi.org/10.1371/journal.pone.0001055
spellingShingle Saliou Fall
Anne Mercier
Franck Bertolla
Alexandra Calteau
Laurent Gueguen
Guy Perrière
Timothy M Vogel
Pascal Simonet
Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.
PLoS ONE
title Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.
title_full Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.
title_fullStr Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.
title_full_unstemmed Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.
title_short Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms.
title_sort horizontal gene transfer regulation in bacteria as a spandrel of dna repair mechanisms
url https://doi.org/10.1371/journal.pone.0001055
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