Emergence of Enteroaggregative Escherichia coli within the ST131 Lineage as a Cause of Extraintestinal Infections

• Published in: mBio 2020-05, Vol.11 (3)
• Main Authors: Boll, Erik J, Overballe-Petersen, Søren, Hasman, Henrik, Roer, Louise, Ng, Kim, Scheutz, Flemming, Hammerum, Anette M, Dungu, Arnold, Hansen, Frank, Johannesen, Thor B, Johnson, Abigail, Nair, Divek T, Lilje, Berit, Hansen, Dennis S, Krogfelt, Karen A, Johnson, Timothy J, Price, Lance B, Johnson, James R, Struve, Carsten, Olesen, Bente, Stegger, Marc
• Format: Article
• Language: English
• Subjects: Anti-Bacterial Agents - pharmacology; Bacteremia - microbiology; Biological Specimen Banks; Clinical Science and Epidemiology; Community-Acquired Infections - microbiology; Denmark; Drug Resistance, Multiple, Bacterial - genetics; E. coli; ESBL; Escherichia coli - drug effects; Escherichia coli - genetics; Escherichia coli - pathogenicity; Escherichia coli Infections - microbiology; Genome, Bacterial; genomic; H27; Humans; Multilocus Sequence Typing; Phylogeny; Plasmids - genetics; resistance; Sequence Analysis, DNA; ST131; Urinary Tract Infections - microbiology; Virulence - genetics; Whole Genome Sequencing; World Health Organization
• ISSN: 2161-2129; 2150-7511
• DOI: 10.1128/mBio.00353-20

sequence type 131 (ST131) is a major cause of urinary and bloodstream infections. Its association with extended-spectrum β-lactamases (ESBLs) significantly complicates treatment. Its best-described component is the rapidly expanding 30Rx clade, containing allele 30 of the type 1 fimbrial adhesin gene This lineage appears to have emerged in the United States and spread around the world in part due to the acquisition of the ESBL-encoding gene and resistance to fluoroquinolones. However, non- 30 ST131 sublineages with other acquired CTX-M-type resistance genes are also emerging. Based on whole-genome analyses, we describe here the presence of an ( ) 27 ST131 sublineage that has recently caused an outbreak of community-acquired bacteremia and recurrent urinary tract infections (UTIs) in Denmark. This sublineage has acquired both a virulence plasmid (pAA) that defines the enteroaggregative (EAEC) diarrheagenic pathotype and multiple genes associated with extraintestinal (ExPEC); combined, these traits have made this particular ST131 sublineage successful at colonizing its human host and causing recurrent UTI. Moreover, using a historic World Health Organization (WHO) collection and publicly available genome sequences, we identified a global 27 EAEC ST131 sublineage that dates back as far as 1998. Most 27 EAEC ST131 isolates harbor pAA or pAA-like plasmids, and our analysis strongly implies a single ancestral acquisition among these isolates. These findings illustrate both the profound plasticity of this important pathogenic ST131 27 sublineage and genetic acquisitions of EAEC-specific virulence traits that likely confer an enhanced ability to cause intestinal colonization. ST131 is an important extraintestinal pathogenic lineage. A signature characteristic of ST131 is its ability to asymptomatically colonize the gastrointestinal tract and then opportunistically cause extraintestinal infections, such as cystitis, pyelonephritis, and urosepsis. In this study, we identified an ST131 27 sublineage that has acquired the enteroaggregative diarrheagenic phenotype, spread across multiple continents, and caused multiple outbreaks of community-acquired ESBL-associated bloodstream infections in Denmark. The strain's ability to both cause diarrhea and innocuously colonize the human gastrointestinal tract may facilitate its dissemination and establishment in the community.