Differential dynamics and impacts of prophages and plasmids on the pangenome and virulence factor repertoires of Shiga toxin-producing Escherichia coli O145:H28

Abstract

Phages and plasmids play important roles in bacterial evolution and diversification. Although many draft genomes have been generated, phage and plasmid genomes are usually fragmented, limiting our understanding of their dynamics. Here, we performed a systematic analysis of 239 draft genomes and 7 complete genomes of Shiga toxin (Stx)-producing Escherichia coli O145:H28, the major virulence factors of which are encoded by prophages (PPs) or plasmids. The results indicated that PPs are more stably maintained than plasmids. A set of ancestrally acquired PPs was well conserved, while various PPs, including Stx phages, were acquired by multiple sublineages. In contrast, gains and losses of a wide range of plasmids have frequently occurred across the O145:H28 lineage, and only the virulence plasmid was well conserved. The different dynamics of PPs and plasmids have differentially impacted the pangenome of O145:H28, with high proportions of PP- and plasmid-associated genes in the variably present and rare gene fractions, respectively. The dynamics of PPs and plasmids have also strongly impacted virulence gene repertoires, such as the highly variable distribution of stx genes and the high conservation of a set of type III secretion effectors, which probably represents the core effectors of O145:H28 and the genes on the virulence plasmid in the entire O145:H28 population. These results provide detailed insights into the dynamics of PPs and plasmids, and show the application of genomic analyses using a large set of draft genomes and appropriately selected complete genomes.

Genomic epidemiology and carbon metabolism of Escherichia coli serogroup O145 reflect contrasting phylogenies

“…The remaining 57 isolates were stx-negative. Similar stx variants were detected in an analysis of 239 O145:H28 strains [44]; however, stx2f was not detected and was only detected in four O145:H34 strains in this study. It has been suggested that different stx variants may have varying levels of virulence, for example, stx2a has been associated with an increased risk of developing HUS [75,76], in comparison stx1 variants were associated with a lower risk [75].…”

“…found to be predominant (230 of 239, 96.2%) in a study of O145:H28 strains [44]. Each ST was also associated with a specific eae subtype, as highlighted in the neighbour-joining tree generated from SNPs identified in 51 genes encoding the ribosome protein subunits (Fig 1).…”

“…Whole genome sequencing (WGS) provides the ability for high-resolution genetic typing analysis that can be used in epidemiological investigations whilst simultaneously providing information on an isolate's gene content. Previous studies to provide STEC serogroup phylogenies have been limited through the analysis of WGS data from a limited number of serogroup-specific strains [41][42][43], or from datasets biased towards human isolates [44], causing wide-ranging serogroup-specific diversity to be over looked.…”

Duplication and diversification of a unique chromosomal virulence island hosting the subtilase cytotoxin in Escherichia coli ST58

“…The capacity to successfully colonize such a broad range of environments stems largely from its ability to acquire and integrate genetic cargo from lateral sources. The acquisition of plasmids [2–4], phagemids [5], phages [4, 6–8] and genomic islands [2, 9] has played an important role in shaping the evolution of E. coli and other clinically important proteobacteria.…”

Genomic network analysis of an environmental and livestock IncF plasmid population

“…This includes livestock [1][2][3][4][5] and water-borne [6] resistance. Frequent horizontal gene transfer (HGT) in Enterobacteriaceae populations results in a large and open pangenome, enabling the wide-spread transmission of the genes conferring AMR [7][8][9]. This includes AMR transmission between humans and the environment and vice versa [10].…”