Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission?

Piklu Roy Chowdhury; Priyanka Hastak; Matthew DeMaere; Ethan Wyrsch; Dmitriy Li; Paarthiphan Elankumaran; Monika Dolejska; Glenn F. Browning; Mark S. Marenda; Thomas Gottlieb; Elaine Cheong; John Merlino; Garry S. A. Myers; Steven P. Djordjevic

doi:10.1128/msystems.01236-22

mSystems (Oct 2023)

Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission?

Piklu Roy Chowdhury,
Priyanka Hastak,
Matthew DeMaere,
Ethan Wyrsch,
Dmitriy Li,
Paarthiphan Elankumaran,
Monika Dolejska,
Glenn F. Browning,
Mark S. Marenda,
Thomas Gottlieb,
Elaine Cheong,
John Merlino,
Garry S. A. Myers,
Steven P. Djordjevic

Affiliations

Piklu Roy Chowdhury: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Priyanka Hastak: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Matthew DeMaere: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Ethan Wyrsch: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Dmitriy Li: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Paarthiphan Elankumaran: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Monika Dolejska: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Glenn F. Browning: Asia-Pacific Centre for Animal Health, Melbourne Veterinary School, University of Melbourne , Parkville, Melbourne, Victoria, Australia
Mark S. Marenda: Asia-Pacific Centre for Animal Health, Melbourne Veterinary School, University of Melbourne , Parkville, Melbourne, Victoria, Australia
Thomas Gottlieb: Department of Microbiology and Infectious Diseases, Concord Hospital and NSW Health Pathology, Hospital Road , Concord, New South Wales, Australia
Elaine Cheong: Department of Microbiology and Infectious Diseases, Concord Hospital and NSW Health Pathology, Hospital Road , Concord, New South Wales, Australia
John Merlino: Department of Microbiology and Infectious Diseases, Concord Hospital and NSW Health Pathology, Hospital Road , Concord, New South Wales, Australia
Garry S. A. Myers: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia
Steven P. Djordjevic: Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, Australia

DOI: https://doi.org/10.1128/msystems.01236-22
Journal volume & issue: Vol. 8, no. 5

Abstract

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ABSTRACT We performed a comprehensive phylogenomic analysis of 925 extraintestinal pathogenic Escherichia coli (ExPEC) ST38 genomes from 38 countries and diverse hosts and sources. The phylogeny resolved two broad clades: A (593 strains; 91% human) and B (332 isolates; 42% human), each with distinct ST38 clusters linked to the carriage of specific bla CTX-M alleles, often in association with other antibiotic resistance genes, class 1 integrons and specific plasmid replicon types. Co-carriage of fyuA and irp2 virulence genes, a reliable proxy for carriage of the Yersinia high-pathogenicity island, featured in 580 (62.7%) genomes. ST38 lineages carrying combinations of ExPEC and intestinal pathogenic Escherichia coli virulence factors were also identified. The F plasmid replicon was identified in 536 (58%) genomes, and 112 of these (21%) carry cjrABC-senB, a virulence operon frequently identified in pandemic ExPEC sequence types. Most (108; 96.4%) cjrABC-senB+ ST38 isolates were from human and other sources, except food animals, and were associated with F5:A-:B10 (41 isolates), F1:A2:B20 (20 isolates), and F24:A-:B1 (15 isolates) F replicon types. ST38 genomes that were inferred to carry a ColV-F virulence plasmid (69; 7.4%) were mostly from human (12; 17.4%), avian (26; 37.7%), or poultry (10; 6.9%) sources. We identified multiple examples of putative inter-host and host-environment transmission events, where genomes differed by <35 SNPs. This work emphasizes the importance of adopting a One Health approach for phylogenomic studies that seek to improve understanding of antimicrobial resistance and pathogen evolution. IMPORTANCE Extraintestinal pathogenic Escherichia coli (ExPEC) sequence type (ST) 38 is one of the top 10 human pandemic lineages. Although a major cause of urinary tract and blood stream infections, ST38 has been poorly characterized from a global phylogenomic perspective. A comprehensive genome-scale analysis of 925 ST38 isolate genomes identified two broad ancestral clades and linkage of discrete ST38 clusters with specific bla CTX-M variants. In addition, the clades and clusters carry important virulence genes, with diverse but poorly characterized plasmids. Numerous putative interhost and environment transmission events were identified here by the presence of ST38 clones (defined as isolates with ≤35 SNPs) within humans, companion animals, food sources, urban birds, wildlife, and the environment. A small cluster of international ST38 clones from diverse sources, likely representing progenitors of a hospital outbreak that occurred in Brisbane, Australia, in 2017, was also identified. Our study emphasizes the importance of characterizing isolate genomes derived from nonhuman sources and geographical locations, without any selection bias.

Published in mSystems

ISSN: 2379-5077 (Online)
Publisher: American Society for Microbiology
Country of publisher: United States
LCC subjects: Science: Microbiology
Website: https://journals.asm.org/journal/msystems

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