An evolutionary analysis of genome expansion and pathogenicity in Escherichia coli.

Jon Bohlin,Camilla Sekse,Ola B Brynildsrud,Lars Snipen

doi:10.1186/1471-2164-15-882

Abstract

BackgroundThere 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.ResultsHierarchical 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, R2~0.98, 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).ConclusionsOn 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 materialThe online version of this article (doi:10.1186/1471-2164-15-882) contains supplementary material, which is available to authorized users.

Highlights

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
Estimation of dN and dS from the E. coli core genome We wanted to explore whether there was a relationship between the selective pressures that the E. coli core genome has been subjected to and genome expansion due to HGT since an association between purifying selection and genome size has previously been identified for microbial species in general [20]
Our findings indicate no correlation between core- and whole genome relative entropy (p ~ 0.26) suggesting that selective pressures operating on the core genome are most likely unrelated to selective forces effective on the rest of the genome

Summary

Introduction

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. We 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. The expected codon frequencies are calculated from genomic nucleotide frequencies so that decreasing distances between observed and expected codon frequencies imply increased independence between the neighboring nucleotides constituting the codons. This implies more random distributions of codon frequencies presumably due to mutations/genetic drift [13,15]. The greater similarity between AT-rich genomes and random DNA sequences, with similar base compositions, is a consequence of the fact that genomic mutations are in general biased towards AT-richness [17,18]

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