Evolutionary History of the Global Emergence of the Escherichia coli Epidemic Clone ST131

Abstract

Escherichia coli sequence type 131 (ST131) has emerged globally as the most predominant extraintestinal pathogenic lineage within this clinically important species, and its association with fluoroquinolone and extended-spectrum cephalosporin resistance impacts significantly on treatment. The evolutionary histories of this lineage, and of important antimicrobial resistance elements within it, remain unclearly defined. This study of the largest worldwide collection (n = 215) of sequenced ST131 E. coli isolates to date demonstrates that the clonal expansion of two previously recognized antimicrobial-resistant clades, C1/H30R and C2/H30Rx, started around 25 years ago, consistent with the widespread introduction of fluoroquinolones and extended-spectrum cephalosporins in clinical medicine. These two clades appear to have emerged in the United States, with the expansion of the C2/H30Rx clade driven by the acquisition of a blaCTX-M-15-containing IncFII-like plasmid that has subsequently undergone extensive rearrangement. Several other evolutionary processes influencing the trajectory of this drug-resistant lineage are described, including sporadic acquisitions of CTX-M resistance plasmids and chromosomal integration of blaCTX-M within subclusters followed by vertical evolution. These processes are also occurring for another family of CTX-M gene variants more recently observed among ST131, the blaCTX-M-14/14-like group. The complexity of the evolutionary history of ST131 has important implications for antimicrobial resistance surveillance, epidemiological analysis, and control of emerging clinical lineages of E. coli. These data also highlight the global imperative to reduce specific antibiotic selection pressures and demonstrate the important and varied roles played by plasmids and other mobile genetic elements in the perpetuation of antimicrobial resistance within lineages.

GlobalEscherichia coliSequence Type 131 Clade withblaCTX-M-27Gene

“…The phylogeny and smaller numbers of SNPs in the C1-M27 clade (Figure 1) suggest that this clade was recently diverged from the C1/ H 30R. In the time-scaled phylogeny presented by Stoesser et al ( 27 ), a cluster that included 6 CTX-M-27–producing isolates from Cambodia, Thailand, and Laos in 2007–2011 was present within the C1/ H 30R clade. This cluster, supposed to be the C1-M27 clade, diverged in the early 2000s, supporting our hypothesis.…”

“…Recent studies focusing on evolutionary history of ST131 suggested that C1/ H 30R and C2/ H 30Rx clades emerged ≈30 years ago, after their acquisition of gyrA -1AB and parC -1aAB alleles from C0/ H 30 (non-R) clade ( 27 , 28 ). The phylogeny and smaller numbers of SNPs in the C1-M27 clade (Figure 1) suggest that this clade was recently diverged from the C1/ H 30R.…”

The ST131 Escherichia coli H22 subclone from human intestinal microbiota: Comparison of genomic and phenotypic traits with those of the globally successful H30 subclone

“…Within this subclone, a subgroup called H 30-Rx, mostly comprising strains resistant to fluoroquinolones and producing CTX-M-15, has quickly emerged and disseminated [2]. The evolutionary history of clone ST131 revealed that before the emergence and dissemination of subclone H 30 (also called clade C), the ST131 population consisted of mostly two subclones called H 22 (clade B) and H 41 (clade A), with subclone H 22 comprised of mostly fluoroquinolone-susceptible isolates [3–5]. It also revealed that subclone H 22 was the precursor of subclone H 30 and that separate F-type plasmids have shaped the evolution of subclone H 30 [2, 3, 5, 6].…”

“…The evolutionary history of clone ST131 revealed that before the emergence and dissemination of subclone H 30 (also called clade C), the ST131 population consisted of mostly two subclones called H 22 (clade B) and H 41 (clade A), with subclone H 22 comprised of mostly fluoroquinolone-susceptible isolates [3–5]. It also revealed that subclone H 22 was the precursor of subclone H 30 and that separate F-type plasmids have shaped the evolution of subclone H 30 [2, 3, 5, 6]. The most recent ST131 E. coli phylogenetic reconstruction carried out by Ben Zakour et al using 3779 non-recombinant single nucleotide polymorphisms (SNP) found in the high quality genomes of 172 clade B and C strains, identified five B subclades, for which the independent evolutionary trajectories are characterized by successive insertions and a recombination from ancestral H 22 (subclade B1) [7].…”

First Report of Group CTX-M-9 Extended Spectrum Beta-Lactamases in Escherichia coli Isolates from Pediatric Patients in Mexico

“…The association of CTX-M-14 and CTX-M-27 with the pandemic clone ST131 has been reported [67]. Recently, the presence of E .…”