Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission?
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...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-10-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01236-22 |
| _version_ | 1797617665735393280 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Piklu Roy Chowdhury |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-11T07:59:01Z |
| format | Article |
| id | doaj.art-afaaf885e93842cd83b45b2ca21ab96b |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-11T07:59:01Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-afaaf885e93842cd83b45b2ca21ab96b2023-11-17T03:22:37ZengAmerican Society for MicrobiologymSystems2379-50772023-10-018510.1128/msystems.01236-22Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission?Piklu Roy Chowdhury0Priyanka Hastak1Matthew DeMaere2Ethan Wyrsch3Dmitriy Li4Paarthiphan Elankumaran5Monika Dolejska6Glenn F. Browning7Mark S. Marenda8Thomas Gottlieb9Elaine Cheong10John Merlino11Garry S. A. Myers12Steven P. Djordjevic13Australian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAsia-Pacific Centre for Animal Health, Melbourne Veterinary School, University of Melbourne , Parkville, Melbourne, Victoria, AustraliaAsia-Pacific Centre for Animal Health, Melbourne Veterinary School, University of Melbourne , Parkville, Melbourne, Victoria, AustraliaDepartment of Microbiology and Infectious Diseases, Concord Hospital and NSW Health Pathology, Hospital Road , Concord, New South Wales, AustraliaDepartment of Microbiology and Infectious Diseases, Concord Hospital and NSW Health Pathology, Hospital Road , Concord, New South Wales, AustraliaDepartment of Microbiology and Infectious Diseases, Concord Hospital and NSW Health Pathology, Hospital Road , Concord, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaAustralian Institute for Microbiology & Infection, University of Technology Sydney, Ultimo , Sydney, New South Wales, AustraliaABSTRACT 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.https://journals.asm.org/doi/10.1128/msystems.01236-22enteroaggregative E. coliEAECST38One Healthbla CTX-Mgenomic surveillance |
| spellingShingle | 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 Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission? mSystems enteroaggregative E. coli EAEC ST38 One Health bla CTX-M genomic surveillance |
| title | Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission? |
| title_full | Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission? |
| title_fullStr | Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission? |
| title_full_unstemmed | Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission? |
| title_short | Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission? |
| title_sort | phylogenomic analysis of a global collection of escherichia coli st38 evidence of interspecies and environmental transmission |
| topic | enteroaggregative E. coli EAEC ST38 One Health bla CTX-M genomic surveillance |
| url | https://journals.asm.org/doi/10.1128/msystems.01236-22 |
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