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Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts

Enteric pathogens cause widespread foodborne illness and are increasingly resistant to important antibiotics yet their ecological impact on the gut microbiome and resistome is not fully understood. Herein, shotgun metagenome sequencing was applied to stool DNA from 60 patients (cases) during an ente...

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Autores principales: Hansen, Zoe A., Vasco, Karla, Rudrik, James T., Scribner, Kim T., Zhang, Lixin, Manning, Shannon D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10509190/
https://www.ncbi.nlm.nih.gov/pubmed/37726374
http://dx.doi.org/10.1038/s41598-023-42822-7
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author Hansen, Zoe A.
Vasco, Karla
Rudrik, James T.
Scribner, Kim T.
Zhang, Lixin
Manning, Shannon D.
author_facet Hansen, Zoe A.
Vasco, Karla
Rudrik, James T.
Scribner, Kim T.
Zhang, Lixin
Manning, Shannon D.
author_sort Hansen, Zoe A.
collection PubMed
description Enteric pathogens cause widespread foodborne illness and are increasingly resistant to important antibiotics yet their ecological impact on the gut microbiome and resistome is not fully understood. Herein, shotgun metagenome sequencing was applied to stool DNA from 60 patients (cases) during an enteric bacterial infection and after recovery (follow-ups). Overall, the case samples harbored more antimicrobial resistance genes (ARGs) with greater resistome diversity than the follow-up samples (p < 0.001), while follow-ups had more diverse gut microbiota (p < 0.001). Although cases were primarily defined by genera Escherichia, Salmonella, and Shigella along with ARGs for multi-compound and multidrug resistance, follow-ups had a greater abundance of Bacteroidetes and Firmicutes phyla and resistance genes for tetracyclines, macrolides, lincosamides, and streptogramins, and aminoglycosides. A host-tracking analysis revealed that Escherichia was the primary bacterial host of ARGs in both cases and follow-ups, with a greater abundance occurring during infection. Eleven distinct extended spectrum beta-lactamase (ESBL) genes were identified during infection, with some detectable upon recovery, highlighting the potential for gene transfer within the community. Because of the increasing incidence of disease caused by foodborne pathogens and their role in harboring and transferring resistance determinants, this study enhances our understanding of how enteric infections impact human gut ecology.
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spelling pubmed-105091902023-09-21 Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts Hansen, Zoe A. Vasco, Karla Rudrik, James T. Scribner, Kim T. Zhang, Lixin Manning, Shannon D. Sci Rep Article Enteric pathogens cause widespread foodborne illness and are increasingly resistant to important antibiotics yet their ecological impact on the gut microbiome and resistome is not fully understood. Herein, shotgun metagenome sequencing was applied to stool DNA from 60 patients (cases) during an enteric bacterial infection and after recovery (follow-ups). Overall, the case samples harbored more antimicrobial resistance genes (ARGs) with greater resistome diversity than the follow-up samples (p < 0.001), while follow-ups had more diverse gut microbiota (p < 0.001). Although cases were primarily defined by genera Escherichia, Salmonella, and Shigella along with ARGs for multi-compound and multidrug resistance, follow-ups had a greater abundance of Bacteroidetes and Firmicutes phyla and resistance genes for tetracyclines, macrolides, lincosamides, and streptogramins, and aminoglycosides. A host-tracking analysis revealed that Escherichia was the primary bacterial host of ARGs in both cases and follow-ups, with a greater abundance occurring during infection. Eleven distinct extended spectrum beta-lactamase (ESBL) genes were identified during infection, with some detectable upon recovery, highlighting the potential for gene transfer within the community. Because of the increasing incidence of disease caused by foodborne pathogens and their role in harboring and transferring resistance determinants, this study enhances our understanding of how enteric infections impact human gut ecology. Nature Publishing Group UK 2023-09-19 /pmc/articles/PMC10509190/ /pubmed/37726374 http://dx.doi.org/10.1038/s41598-023-42822-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hansen, Zoe A.
Vasco, Karla
Rudrik, James T.
Scribner, Kim T.
Zhang, Lixin
Manning, Shannon D.
Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts
title Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts
title_full Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts
title_fullStr Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts
title_full_unstemmed Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts
title_short Recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts
title_sort recovery of the gut microbiome following enteric infection and persistence of antimicrobial resistance genes in specific microbial hosts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10509190/
https://www.ncbi.nlm.nih.gov/pubmed/37726374
http://dx.doi.org/10.1038/s41598-023-42822-7
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