To kill or to be killed: pangenome analysis of Escherichia coli strains reveals a tailocin specific for pandemic ST131

Abstract

AbstractBackgroundEscherichia coli(E. coli) has been one of the most studied model organisms in the history of life sciences. Initially thought just to be commensal bacteria,E. colihas shown wide phenotypic diversity including pathogenic isolates with great relevance to public health. Though pangenome analysis has been attempted several times, there is no systematic functional characterization of theE. colisubgroups according to the gene profile.ResultsSystematically scanning for optimal parametrization, we have built theE. colipangenome from 1324 complete genomes. The pangenome size is estimated to be ~25,000 gene families (GFs). Whereas the core genome diminishes as more genomes are added, the softcore genome (≥95% of strains) is stable with ~3000 GFs regardless of the total number of genomes. Apparently, the softcore genome (with a 92% or 95% generation threshold) can define the genome of a bacterial species listing the critically relevant, evolutionarily most conserved or important classes of GFs. Unsupervised clustering of commonE. colisequence types using the presence/absence GF matrix reveals distinct characteristics ofE. coliphylogroups B1, B2, and E. We highlight the bi-lineage nature of B1, the variation of the secretion and of the iron acquisition systems in ST11 (E), and the incorporation of a highly conserved prophage into the genome of ST131 (B2). The tail structure of the prophage is evolutionarily related to R2-pyocin (a tailocin) fromPseudomonas aeruginosaPAO1. We hypothesize that this molecular machinery is highly likely to play an important role in protecting its own colonies; thus, contributing towards the rapid rise of pandemicE. coliST131.ConclusionsThis study has explored the optimized pangenome development inE. coli. We provide complete GF lists and the pangenome matrix as supplementary data for further studies. We identified biological characteristics of differentE. colisubtypes, specifically for phylogroups B1, B2, and E. We found an operon-like genome region coding for a tailocin specific for ST131 strains. The latter is a potential killer weapon providing pandemicE. coliST131 with an advantage in inter-bacterial competition and, suggestively, explains their dominance as human pathogen amongE. colistrains.