Phylogroup stability contrasts with high within sequence type complex dynamics of Escherichia coli bloodstream infection isolates over a 12-year period

Abstract

Background Escherichia coli is the leading cause of bloodstream infections, associated with a significant mortality. Recent genomic analyses revealed that few clonal lineages are involved in bloodstream infections and captured the emergence of some of them. However, data on within sequence type (ST) population genetic structure evolution are rare. Methods We compared whole genome sequences of 912 E. coli isolates responsible for bloodstream infections from two multicenter clinical trials that were conducted in the Paris area, France, 12 years apart, in teaching hospitals belonging to the same institution (“Assistance Publique-Hôpitaux de Paris”). We analyzed the strains at different levels of granularity, i.e., the phylogroup, the ST complex (STc), and the within STc clone taking into consideration the evolutionary history, the resistance, and virulence gene content as well as the antigenic diversity of the strains. Results We found a mix of stability and changes overtime, depending on the level of comparison. Overall, we observed an increase in antibiotic resistance associated to a restricted number of genetic determinants and in strain plasmidic content, whereas phylogroup distribution and virulence gene content remained constant. Focusing on STcs highlighted the pauci-clonality of the populations, with only 11 STcs responsible for more than 73% of the cases, dominated by five STcs (STc73, STc131, STc95, STc69, STc10). However, some STcs underwent dramatic variations, such as the global pandemic STc131, which replaced the previously predominant STc95. Moreover, within STc131, 95 and 69 genomic diversity analysis revealed a highly dynamic pattern, with reshuffling of the population linked to clonal replacement sometimes coupled with independent acquisitions of virulence factors such as the pap gene cluster bearing a papGII allele located on various pathogenicity islands. Additionally, STc10 exhibited huge antigenic diversity evidenced by numerous O:H serotype/fimH allele combinations, whichever the year of isolation. Conclusions Altogether, these data suggest that the bloodstream niche is occupied by a wide but specific phylogenetic diversity and that highly specialized extra-intestinal clones undergo frequent turnover at the within ST level. Additional worldwide epidemiological studies overtime are needed in different geographical and ecological contexts to assess how generalizable these data are.

Genome Informatics and Machine Learning-Based Identification of Antimicrobial Resistance-Encoding Features and Virulence Attributes in Escherichia coli Genomes Representing Globally Prevalent Lineages, Including High-Risk Clonal Complexes

“…With a curated data set of 5,653 E. coli genomes, we attempted to identify and understand the involvement of different genomic features with a plausible role in the evolution of 19 different ST lineages with varied pathogenic, resistance, and fitness capabilities, some bearing high risk of transmission with pandemic potentials. ST10 from our study has shown a wide serotype diversity, wherein its 1,036 genomes belonged to 222 serotypes; this is in agreement with a previous report ( 32 ). While a majority of the sequence types revealed a very high antigenic diversity, a few STs, such as ST131, ST11, ST405, and ST127, showed limited antigenic diversity where more than 80% of the genomes belonging to these STs represented a single serotype.…”

Prevalence, Risk Factors, and Genetic Characterization of Extended-Spectrum Beta-Lactamase Escherichia coli Isolated From Healthy Pregnant Women in Madagascar

“…STc155 strains are considered of animal origin with an evolution from wild type strains, becoming progressively resistant and, in many cases, later acquiring virulence genes (Skurnik et al, 2016). Indeed, in recent years multi-drug resistant (MDR) STc155 strains have been isolated with increasing frequency from extra-intestinal infections in humans (Royer et al, 2021). In our study STc155 isolates carried only a limited number of virulence genes but had already acquired an MDR profile.…”

A role for ColV plasmids in the evolution of pathogenic Escherichia coli ST58

“…The major question remaining is whether most ST58 from human faeces and ExPEC belong to the BAP2 cluster. Though not included in our study collection, ST58 sepsis isolates from multiple hospitals in Paris predominantly display O8/O9:H25 serotypes, as well as ColV and HPI marker genes, all of which were typical of BAP2 ST58 3 . In conjunction with our data, this tends to suggest that most ST58 ExPEC will belong to this cluster, however, an expanded dataset with more commensal and pathogenic human sequences would increase our confidence.…”

“…Most ExPEC strains, including those in the globally dominant ST131 clonal group, are members of phylogroup B2 2 . The emergence of ST58 is perhaps best highlighted by a recent study that found the proportion of B1-ST58 isolated from bloodstream infections in the Paris region has more than doubled over a 12 year period in contrast to stable proportions of infections caused by phylogroup B2 isolates 3 . Beyond this study, E. coli ST58 is increasingly responsible for both sporadic and persistent cases of bloodstream infections in humans across the globe 4 – 12 .…”