Phylogenetic background and habitat drive the genetic diversification of Escherichia coli.

Marie Touchon,Erick Denamur,David Gordon,Claire L O’Brien,Belinda Vangchhia,Jorge André Moura De Sousa,Eduardo Pc Rocha,Samantha Burn,Amandine Perrin,Xavier Didelot

doi:10.1371/journal.pgen.1008866

Abstract

Escherichia coli is mostly a commensal of birds and mammals, including humans, where it can act as an opportunistic pathogen. It is also found in water and sediments. We investigated the phylogeny, genetic diversification, and habitat-association of 1,294 isolates representative of the phylogenetic diversity of more than 5,000 isolates from the Australian continent. Since many previous studies focused on clinical isolates, we investigated mostly other isolates originating from humans, poultry, wild animals and water. These strains represent the species genetic diversity and reveal widespread associations between phylogroups and isolation sources. The analysis of strains from the same sequence types revealed very rapid change of gene repertoires in the very early stages of divergence, driven by the acquisition of many different types of mobile genetic elements. These elements also lead to rapid variations in genome size, even if few of their genes rise to high frequency in the species. Variations in genome size are associated with phylogroup and isolation sources, but the latter determine the number of MGEs, a marker of recent transfer, suggesting that gene flow reinforces the association of certain genetic backgrounds with specific habitats. After a while, the divergence of gene repertoires becomes linear with phylogenetic distance, presumably reflecting the continuous turnover of mobile element and the occasional acquisition of adaptive genes. Surprisingly, the phylogroups with smallest genomes have the highest rates of gene repertoire diversification and fewer but more diverse mobile genetic elements. This suggests that smaller genomes are associated with higher, not lower, turnover of genetic information. Many of these genomes are from freshwater isolates and have peculiar traits, including a specific capsule, suggesting adaptation to this environment. Altogether, these data contribute to explain why epidemiological clones tend to emerge from specific phylogenetic groups in the presence of pervasive horizontal gene transfer across the species.

Highlights

The integration of epidemiology and genomics has greatly contributed to our understanding of the population genetics of epidemic clones of pathogenic bacteria
Previous large scale studies on the evolution of E. coli focused on clinical isolates emphasizing virulence and antibiotic resistance in medically important lineages
We analyzed a large collection of non-clinical isolates of the species to assess the mechanisms of gene repertoire diversification in the light of isolation sources and phylogeny

Summary

Introduction

The integration of epidemiology and genomics has greatly contributed to our understanding of the population genetics of epidemic clones of pathogenic bacteria. Some E. coli strains produce virulence factors endowing them with the ability to cause a broad range of intestinal or extraintestinal diseases (pathotypes) in humans and domestic animals [8,9,10,11,12,13]. Studies on E. coli were seminal in the development of bacterial population genetics [16] They showed moderate levels of recombination in the species [3, 17,18,19], and a strong phylogenetic structure with eight main phylogroups, among which four (A, B1, B2 and D) represent the majority of the strains and four others (C, E, F and G) are rarer [20,21,22]. Genome size differs among phylogroups, with A and B1 strains having smaller genomes than B2 or D strains [23]

Methods

Results

Discussion

Conclusion