GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands

The characterization of functional elements in genomes relies on the identification of the footprints of natural selection. In this quest, taking into account neutral evolutionary processes such as mutation and genetic drift is crucial because these forces can generate patterns that may obscure or m...

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Main Authors:	Lassalle, Florent, Périan, Séverine, Bataillon, Thomas, Nesme, Xavier, Duret, Laurent, Daubin, Vincent
Format:	Online
Language:	English
Published:	Public Library of Science 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4450053/

id	pubmed-4450053
recordtype	oai_dc
spelling	pubmed-44500532015-06-23 GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands Lassalle, Florent Périan, Séverine Bataillon, Thomas Nesme, Xavier Duret, Laurent Daubin, Vincent Research Article The characterization of functional elements in genomes relies on the identification of the footprints of natural selection. In this quest, taking into account neutral evolutionary processes such as mutation and genetic drift is crucial because these forces can generate patterns that may obscure or mimic signatures of selection. In mammals, and probably in many eukaryotes, another such confounding factor called GC-Biased Gene Conversion (gBGC) has been documented. This mechanism generates patterns identical to what is expected under selection for higher GC-content, specifically in highly recombining genomic regions. Recent results have suggested that a mysterious selective force favouring higher GC-content exists in Bacteria but the possibility that it could be gBGC has been excluded. Here, we show that gBGC is probably at work in most if not all bacterial species. First we find a consistent positive relationship between the GC-content of a gene and evidence of intra-genic recombination throughout a broad spectrum of bacterial clades. Second, we show that the evolutionary force responsible for this pattern is acting independently from selection on codon usage, and could potentially interfere with selection in favor of optimal AU-ending codons. A comparison with data from human populations shows that the intensity of gBGC in Bacteria is comparable to what has been reported in mammals. We propose that gBGC is not restricted to sexual Eukaryotes but also widespread among Bacteria and could therefore be an ancestral feature of cellular organisms. We argue that if gBGC occurs in bacteria, it can account for previously unexplained observations, such as the apparent non-equilibrium of base substitution patterns and the heterogeneity of gene composition within bacterial genomes. Because gBGC produces patterns similar to positive selection, it is essential to take this process into account when studying the evolutionary forces at work in bacterial genomes. Public Library of Science 2015-02-06 /pmc/articles/PMC4450053/ /pubmed/25659072 http://dx.doi.org/10.1371/journal.pgen.1004941 Text en © 2015 Lassalle et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Lassalle, Florent Périan, Séverine Bataillon, Thomas Nesme, Xavier Duret, Laurent Daubin, Vincent
spellingShingle	Lassalle, Florent Périan, Séverine Bataillon, Thomas Nesme, Xavier Duret, Laurent Daubin, Vincent GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands
author_facet	Lassalle, Florent Périan, Séverine Bataillon, Thomas Nesme, Xavier Duret, Laurent Daubin, Vincent
author_sort	Lassalle, Florent
title	GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands
title_short	GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands
title_full	GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands
title_fullStr	GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands
title_full_unstemmed	GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands
title_sort	gc-content evolution in bacterial genomes: the biased gene conversion hypothesis expands
description	The characterization of functional elements in genomes relies on the identification of the footprints of natural selection. In this quest, taking into account neutral evolutionary processes such as mutation and genetic drift is crucial because these forces can generate patterns that may obscure or mimic signatures of selection. In mammals, and probably in many eukaryotes, another such confounding factor called GC-Biased Gene Conversion (gBGC) has been documented. This mechanism generates patterns identical to what is expected under selection for higher GC-content, specifically in highly recombining genomic regions. Recent results have suggested that a mysterious selective force favouring higher GC-content exists in Bacteria but the possibility that it could be gBGC has been excluded. Here, we show that gBGC is probably at work in most if not all bacterial species. First we find a consistent positive relationship between the GC-content of a gene and evidence of intra-genic recombination throughout a broad spectrum of bacterial clades. Second, we show that the evolutionary force responsible for this pattern is acting independently from selection on codon usage, and could potentially interfere with selection in favor of optimal AU-ending codons. A comparison with data from human populations shows that the intensity of gBGC in Bacteria is comparable to what has been reported in mammals. We propose that gBGC is not restricted to sexual Eukaryotes but also widespread among Bacteria and could therefore be an ancestral feature of cellular organisms. We argue that if gBGC occurs in bacteria, it can account for previously unexplained observations, such as the apparent non-equilibrium of base substitution patterns and the heterogeneity of gene composition within bacterial genomes. Because gBGC produces patterns similar to positive selection, it is essential to take this process into account when studying the evolutionary forces at work in bacterial genomes.
publisher	Public Library of Science
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4450053/
_version_	1613229856161529856

GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands

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