The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice

Abstract Background Emergence of antibiotic resistance is a global public health concern. The relationships between antibiotic use, the gut community composition, normal physiology and metabolism, and individual and public health are still being defined. Shifts in composition of bacteria, antibiotic...

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Main Authors: Lei Xu, Anil Surathu, Isaac Raplee, Ashok Chockalingam, Sharron Stewart, Lacey Walker, Leonard Sacks, Vikram Patel, Zhihua Li, Rodney Rouse
Format: Article
Language:English
Published: BMC 2020-03-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-6665-2
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record_format Article
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language English
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author Lei Xu
Anil Surathu
Isaac Raplee
Ashok Chockalingam
Sharron Stewart
Lacey Walker
Leonard Sacks
Vikram Patel
Zhihua Li
Rodney Rouse
spellingShingle Lei Xu
Anil Surathu
Isaac Raplee
Ashok Chockalingam
Sharron Stewart
Lacey Walker
Leonard Sacks
Vikram Patel
Zhihua Li
Rodney Rouse
The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
BMC Genomics
Gut microbiome
Next generation sequencing
Antibiotics
Antibiotic resistance
Metagenome
author_facet Lei Xu
Anil Surathu
Isaac Raplee
Ashok Chockalingam
Sharron Stewart
Lacey Walker
Leonard Sacks
Vikram Patel
Zhihua Li
Rodney Rouse
author_sort Lei Xu
title The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
title_short The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
title_full The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
title_fullStr The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
title_full_unstemmed The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
title_sort effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2020-03-01
description Abstract Background Emergence of antibiotic resistance is a global public health concern. The relationships between antibiotic use, the gut community composition, normal physiology and metabolism, and individual and public health are still being defined. Shifts in composition of bacteria, antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) after antibiotic treatment are not well-understood. Methods This project used next-generation sequencing, custom-built metagenomics pipeline and differential abundance analysis to study the effect of antibiotic monotherapy on resistome and taxonomic composition in the gut of Balb/c mice infected with E. coli via transurethral catheterization to investigate the evolution and emergence of antibiotic resistance. Results There is a longitudinal decrease of gut microbiota diversity after antibiotic treatment. Various ARGs are enriched within the gut microbiota despite an overall reduction of the diversity and total amount of bacteria after antibiotic treatment. Sometimes treatment with a specific class of antibiotics selected for ARGs that resist antibiotics of a completely different class (e.g. treatment of ciprofloxacin or fosfomycin selected for cepA that resists ampicillin). Relative abundance of some MGEs increased substantially after antibiotic treatment (e.g. transposases in the ciprofloxacin group). Conclusions Antibiotic treatment caused a remarkable reduction in diversity of gut bacterial microbiota but enrichment of certain types of ARGs and MGEs. These results demonstrate an emergence of cross-resistance as well as a profound change in the gut resistome following oral treatment of antibiotics.
topic Gut microbiome
Next generation sequencing
Antibiotics
Antibiotic resistance
Metagenome
url http://link.springer.com/article/10.1186/s12864-020-6665-2
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spelling doaj-bb1a7802bc2f419eaedbedcd570d2a6f2020-11-25T02:12:53ZengBMCBMC Genomics1471-21642020-03-0121111810.1186/s12864-020-6665-2The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated miceLei Xu0Anil Surathu1Isaac Raplee2Ashok Chockalingam3Sharron Stewart4Lacey Walker5Leonard Sacks6Vikram Patel7Zhihua Li8Rodney Rouse9U. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Medical Policy, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterU. S. Food and Drug Administration, Center for Drug Evaluation and Research, Office of Translational Science, Office of Clinical Pharmacology, Division of Applied Regulatory Science, HFD-910, White Oak Federal Research CenterAbstract Background Emergence of antibiotic resistance is a global public health concern. The relationships between antibiotic use, the gut community composition, normal physiology and metabolism, and individual and public health are still being defined. Shifts in composition of bacteria, antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) after antibiotic treatment are not well-understood. Methods This project used next-generation sequencing, custom-built metagenomics pipeline and differential abundance analysis to study the effect of antibiotic monotherapy on resistome and taxonomic composition in the gut of Balb/c mice infected with E. coli via transurethral catheterization to investigate the evolution and emergence of antibiotic resistance. Results There is a longitudinal decrease of gut microbiota diversity after antibiotic treatment. Various ARGs are enriched within the gut microbiota despite an overall reduction of the diversity and total amount of bacteria after antibiotic treatment. Sometimes treatment with a specific class of antibiotics selected for ARGs that resist antibiotics of a completely different class (e.g. treatment of ciprofloxacin or fosfomycin selected for cepA that resists ampicillin). Relative abundance of some MGEs increased substantially after antibiotic treatment (e.g. transposases in the ciprofloxacin group). Conclusions Antibiotic treatment caused a remarkable reduction in diversity of gut bacterial microbiota but enrichment of certain types of ARGs and MGEs. These results demonstrate an emergence of cross-resistance as well as a profound change in the gut resistome following oral treatment of antibiotics.http://link.springer.com/article/10.1186/s12864-020-6665-2Gut microbiomeNext generation sequencingAntibioticsAntibiotic resistanceMetagenome