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An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli

BACKGROUND: There are several studies describing loss of genes through reductive evolution in microbes, but how selective forces are associated with genome expansion due to horizontal gene transfer (HGT) has not received similar attention. The aim of this study was therefore to examine how selective...

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Autores principales: Bohlin, Jon, Brynildsrud, Ola B, Sekse, Camilla, Snipen, Lars
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4200225/
https://www.ncbi.nlm.nih.gov/pubmed/25297974
http://dx.doi.org/10.1186/1471-2164-15-882
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author Bohlin, Jon
Brynildsrud, Ola B
Sekse, Camilla
Snipen, Lars
author_facet Bohlin, Jon
Brynildsrud, Ola B
Sekse, Camilla
Snipen, Lars
author_sort Bohlin, Jon
collection PubMed
description BACKGROUND: There are several studies describing loss of genes through reductive evolution in microbes, but how selective forces are associated with genome expansion due to horizontal gene transfer (HGT) has not received similar attention. The aim of this study was therefore to examine how selective pressures influence genome expansion in 53 fully sequenced and assembled Escherichia coli strains. We also explored potential connections between genome expansion and the attainment of virulence factors. This was performed using estimations of several genomic parameters such as AT content, genomic drift (measured using relative entropy), genome size and estimated HGT size, which were subsequently compared to analogous parameters computed from the core genome consisting of 1729 genes common to the 53 E. coli strains. Moreover, we analyzed how selective pressures (quantified using relative entropy and dN/dS), acting on the E. coli core genome, influenced lineage and phylogroup formation. RESULTS: Hierarchical clustering of dS and dN estimations from the E. coli core genome resulted in phylogenetic trees with topologies in agreement with known E. coli taxonomy and phylogroups. High values of dS, compared to dN, indicate that the E. coli core genome has been subjected to substantial purifying selection over time; significantly more than the non-core part of the genome (p<0.001). This is further supported by a linear association between strain-wise dS and dN values (β = 26.94 ± 0.44, R(2)~0.98, p<0.001). The non-core part of the genome was also significantly more AT-rich (p<0.001) than the core genome and E. coli genome size correlated with estimated HGT size (p<0.001). In addition, genome size (p<0.001), AT content (p<0.001) as well as estimated HGT size (p<0.005) were all associated with the presence of virulence factors, suggesting that pathogenicity traits in E. coli are largely attained through HGT. No associations were found between selective pressures operating on the E. coli core genome, as estimated using relative entropy, and genome size (p~0.98). CONCLUSIONS: On a larger time frame, genome expansion in E. coli, which is significantly associated with the acquisition of virulence factors, appears to be independent of selective forces operating on the core genome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-882) contains supplementary material, which is available to authorized users.
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spelling pubmed-42002252014-10-18 An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli Bohlin, Jon Brynildsrud, Ola B Sekse, Camilla Snipen, Lars BMC Genomics Research Article BACKGROUND: There are several studies describing loss of genes through reductive evolution in microbes, but how selective forces are associated with genome expansion due to horizontal gene transfer (HGT) has not received similar attention. The aim of this study was therefore to examine how selective pressures influence genome expansion in 53 fully sequenced and assembled Escherichia coli strains. We also explored potential connections between genome expansion and the attainment of virulence factors. This was performed using estimations of several genomic parameters such as AT content, genomic drift (measured using relative entropy), genome size and estimated HGT size, which were subsequently compared to analogous parameters computed from the core genome consisting of 1729 genes common to the 53 E. coli strains. Moreover, we analyzed how selective pressures (quantified using relative entropy and dN/dS), acting on the E. coli core genome, influenced lineage and phylogroup formation. RESULTS: Hierarchical clustering of dS and dN estimations from the E. coli core genome resulted in phylogenetic trees with topologies in agreement with known E. coli taxonomy and phylogroups. High values of dS, compared to dN, indicate that the E. coli core genome has been subjected to substantial purifying selection over time; significantly more than the non-core part of the genome (p<0.001). This is further supported by a linear association between strain-wise dS and dN values (β = 26.94 ± 0.44, R(2)~0.98, p<0.001). The non-core part of the genome was also significantly more AT-rich (p<0.001) than the core genome and E. coli genome size correlated with estimated HGT size (p<0.001). In addition, genome size (p<0.001), AT content (p<0.001) as well as estimated HGT size (p<0.005) were all associated with the presence of virulence factors, suggesting that pathogenicity traits in E. coli are largely attained through HGT. No associations were found between selective pressures operating on the E. coli core genome, as estimated using relative entropy, and genome size (p~0.98). CONCLUSIONS: On a larger time frame, genome expansion in E. coli, which is significantly associated with the acquisition of virulence factors, appears to be independent of selective forces operating on the core genome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-882) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-09 /pmc/articles/PMC4200225/ /pubmed/25297974 http://dx.doi.org/10.1186/1471-2164-15-882 Text en © Bohlin et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Bohlin, Jon
Brynildsrud, Ola B
Sekse, Camilla
Snipen, Lars
An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli
title An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli
title_full An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli
title_fullStr An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli
title_full_unstemmed An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli
title_short An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli
title_sort evolutionary analysis of genome expansion and pathogenicity in escherichia coli
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4200225/
https://www.ncbi.nlm.nih.gov/pubmed/25297974
http://dx.doi.org/10.1186/1471-2164-15-882
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