Emergence of enteroaggregative escherichia coli within the ST131 lineage as a cause of extraintestinal infections

Erik J. Boll, Søren Overballe-Petersen, Henrik Hasman, Louise Roer, Kim Ng, Flemming Scheutz, Anette M. Hammerum, Arnold Dungu, Frank Hansen, Thor B. Johannesen, Abigail Johnson, Divek T. Nair, Berit Lilje, Dennis S. Hansen, Karen A. Krogfelt, Timothy J. Johnson, Lance B. Price, James R. Johnson, Carsten Struve, Bente OlesenMarc Stegger

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Escherichia coli sequence type 131 (ST131) is a major cause of urinary and bloodstream infections. Its association with extended-spectrum ß-lactamases (ESBLs) significantly complicates treatment. Its best-described component is the rap-idly expanding H30Rx clade, containing allele 30 of the type 1 fimbrial adhesin gene fimH. 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 blaCTX-M-15 gene and resistance to fluoroquinolones. However, non-H30 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 (fimH) H27 E. coli 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 E. coli (EAEC) diarrhea-genic pathotype and multiple genes associated with extraintestinal E. coli (ExPEC); combined, these traits have made this particular ST131 sublineage successful at col-onizing its human host and causing recurrent UTI. Moreover, using a historic World Health Organization (WHO) E. coli collection and publicly available genome se-quences, we identified a global H27 EAEC ST131 sublineage that dates back as far as 1998. Most H27 EAEC ST131 isolates harbor pAA or pAA-like plasmids, and our analysis strongly implies a single ancestral acquisition among these isolates. These find-ings illustrate both the profound plasticity of this important pathogenic E. coli ST131 H27 sublineage and genetic acquisitions of EAEC-specific virulence traits that likely confer an enhanced ability to cause intestinal colonization. IMPORTANCE E. coli ST131 is an important extraintestinal pathogenic lineage. A sig-nature characteristic of ST131 is its ability to asymptomatically colonize the gastrointestinal tract and then opportunistically cause extraintestinal infections, such as cystitis, pye-lonephritis, and urosepsis. In this study, we identified an ST131 H27 sublineage that has acquired the enteroaggregative diarrheagenic phenotype, spread across multiple conti-nents, 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.

Original languageEnglish (US)
Article numbere00353-20
JournalmBio
Volume11
Issue number3
DOIs
StatePublished - 2020

Bibliographical note

Funding Information:
We thank Michala T. Sørensen at Statens Serum Institut for performing the plasmid gel electrophoresis. We also thank Karin Sixhøj Pedersen at Statens Serum Institut for her excellent WGS work. This work was supported financially by the Danish Council for Research, grant DFF-1331-00161, to C. Struve, and the Danish Ministry of Health as part of the Integrated Surveillance of ESBL/AmpC-Producing E. coli and Carbapenemase-Producing Bacteria. This work was also supported in part by the Office of Research and Development, U.S. Department of Veterans Affairs, grant number 2I01CX000920-04, to J. R. Johnson.

Publisher Copyright:
© 2020 Boll et al.

Keywords

  • E. Coli
  • ESBL
  • Enteroaggregative
  • Evolution
  • Genomic
  • H27
  • Outbreak
  • Plasmids
  • Resistance
  • ST131

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