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Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence
Antibiotic therapy is the standard of care for urinary tract infections (UTIs) caused by uropathogenic Escherichia coli (UPEC). However, previous antibiotic therapy may impart a selective pressure that influences the population structure and pathogenic potential of infecting UPEC strains. Here, we c...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433818/ https://www.ncbi.nlm.nih.gov/pubmed/37338386 http://dx.doi.org/10.1128/spectrum.05242-22 |
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author | Ballash, Gregory A. Diaz-Campos, Dubraska van Balen, Joany C. Mollenkopf, Dixie F. Wittum, Thomas E. |
author_facet | Ballash, Gregory A. Diaz-Campos, Dubraska van Balen, Joany C. Mollenkopf, Dixie F. Wittum, Thomas E. |
author_sort | Ballash, Gregory A. |
collection | PubMed |
description | Antibiotic therapy is the standard of care for urinary tract infections (UTIs) caused by uropathogenic Escherichia coli (UPEC). However, previous antibiotic therapy may impart a selective pressure that influences the population structure and pathogenic potential of infecting UPEC strains. Here, we conducted a 3-year study using whole-genome-sequencing analysis and retrospective medical record review to characterize how antibiotic exposure influenced the phenotypic antibiotic resistance, acquired resistome, virulome, and population structure of 88 UTI-causing E. coli strains from dogs. A majority of UTI-associated E. coli strains were from phylogroup B2 and clustered within sequence type 372. Previous antibiotic exposure was associated with a population shift toward UPEC from phylogroups other than the typical urovirulent phylogroup B2. The specific virulence profiles within the accessory virulome that were associated with antibiotic use were elicited by the effect of antibiotics on UPEC phylogenetic structure. Among phylogroup B2, antibiotic exposure increased the quantity of genes within the resistome and the odds of developing reduced susceptibility to at least one antibiotic. Non-B2 UPEC strains harbored a more diverse and greater resistome that conferred reduced susceptibility to multiple antibiotic classes following antibiotic exposure. Collectively, these data suggest that previous antibiotic exposure establishes an environment that provides a selective edge to non-B2 UPEC strains through their diverse and abundant antibiotic resistance genes, despite their lack of urovirulence genes. Our findings highlight the necessity for judicious use of antibiotics as we uncover another mechanism by which antibiotic exposure and resistance can influence the dynamics of bacterial infectious disease. IMPORTANCE Urinary tract infections (UTIs) are one of the most common infections of dogs and humans. While antibiotic therapy is the standard of care for UTIs and other infections, antibiotic exposure may influence the pathogenic profile of subsequent infections. We used whole-genome sequencing and retrospective medical record review to characterize the effect of systemic antibiotic therapy on the resistance, virulence, and population structure of 88 UTI-causing UPEC strains isolated from dogs. Our results indicate that antibiotic exposure alters the population structure of infecting UPEC strains, providing a selective edge for non-B2 phylogroups that harbor diverse and abundant resistance gene catalogues but fewer urovirulence genes. These findings highlight how antibiotic resistance can influence pathogen infection dynamics and have clinical implications for the judicious use of antibiotics for bacterial infections. |
format | Online Article Text |
id | pubmed-10433818 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-104338182023-08-18 Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence Ballash, Gregory A. Diaz-Campos, Dubraska van Balen, Joany C. Mollenkopf, Dixie F. Wittum, Thomas E. Microbiol Spectr Research Article Antibiotic therapy is the standard of care for urinary tract infections (UTIs) caused by uropathogenic Escherichia coli (UPEC). However, previous antibiotic therapy may impart a selective pressure that influences the population structure and pathogenic potential of infecting UPEC strains. Here, we conducted a 3-year study using whole-genome-sequencing analysis and retrospective medical record review to characterize how antibiotic exposure influenced the phenotypic antibiotic resistance, acquired resistome, virulome, and population structure of 88 UTI-causing E. coli strains from dogs. A majority of UTI-associated E. coli strains were from phylogroup B2 and clustered within sequence type 372. Previous antibiotic exposure was associated with a population shift toward UPEC from phylogroups other than the typical urovirulent phylogroup B2. The specific virulence profiles within the accessory virulome that were associated with antibiotic use were elicited by the effect of antibiotics on UPEC phylogenetic structure. Among phylogroup B2, antibiotic exposure increased the quantity of genes within the resistome and the odds of developing reduced susceptibility to at least one antibiotic. Non-B2 UPEC strains harbored a more diverse and greater resistome that conferred reduced susceptibility to multiple antibiotic classes following antibiotic exposure. Collectively, these data suggest that previous antibiotic exposure establishes an environment that provides a selective edge to non-B2 UPEC strains through their diverse and abundant antibiotic resistance genes, despite their lack of urovirulence genes. Our findings highlight the necessity for judicious use of antibiotics as we uncover another mechanism by which antibiotic exposure and resistance can influence the dynamics of bacterial infectious disease. IMPORTANCE Urinary tract infections (UTIs) are one of the most common infections of dogs and humans. While antibiotic therapy is the standard of care for UTIs and other infections, antibiotic exposure may influence the pathogenic profile of subsequent infections. We used whole-genome sequencing and retrospective medical record review to characterize the effect of systemic antibiotic therapy on the resistance, virulence, and population structure of 88 UTI-causing UPEC strains isolated from dogs. Our results indicate that antibiotic exposure alters the population structure of infecting UPEC strains, providing a selective edge for non-B2 phylogroups that harbor diverse and abundant resistance gene catalogues but fewer urovirulence genes. These findings highlight how antibiotic resistance can influence pathogen infection dynamics and have clinical implications for the judicious use of antibiotics for bacterial infections. American Society for Microbiology 2023-06-20 /pmc/articles/PMC10433818/ /pubmed/37338386 http://dx.doi.org/10.1128/spectrum.05242-22 Text en Copyright © 2023 Ballash et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Ballash, Gregory A. Diaz-Campos, Dubraska van Balen, Joany C. Mollenkopf, Dixie F. Wittum, Thomas E. Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence |
title | Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence |
title_full | Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence |
title_fullStr | Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence |
title_full_unstemmed | Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence |
title_short | Previous Antibiotic Exposure Reshapes the Population Structure of Infecting Uropathogenic Escherichia coli Strains by Selecting for Antibiotic Resistance over Urovirulence |
title_sort | previous antibiotic exposure reshapes the population structure of infecting uropathogenic escherichia coli strains by selecting for antibiotic resistance over urovirulence |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433818/ https://www.ncbi.nlm.nih.gov/pubmed/37338386 http://dx.doi.org/10.1128/spectrum.05242-22 |
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