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Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits

Reducing antibiotic use is a necessary step toward less antibiotic resistance in livestock, but many antibiotic resistance genes can persist for years, even in an antibiotic-free environment. In this study, we investigated the potential of three fecal complex microbial communities from antibiotic-na...

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Autores principales: Achard, Caroline Stéphanie, Dupouy, Véronique, Siviglia, Suzanne, Arpaillange, Nathalie, Cauquil, Laurent, Bousquet-Mélou, Alain, Zemb, Olivier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6615258/
https://www.ncbi.nlm.nih.gov/pubmed/31333614
http://dx.doi.org/10.3389/fmicb.2019.01503
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author Achard, Caroline Stéphanie
Dupouy, Véronique
Siviglia, Suzanne
Arpaillange, Nathalie
Cauquil, Laurent
Bousquet-Mélou, Alain
Zemb, Olivier
author_facet Achard, Caroline Stéphanie
Dupouy, Véronique
Siviglia, Suzanne
Arpaillange, Nathalie
Cauquil, Laurent
Bousquet-Mélou, Alain
Zemb, Olivier
author_sort Achard, Caroline Stéphanie
collection PubMed
description Reducing antibiotic use is a necessary step toward less antibiotic resistance in livestock, but many antibiotic resistance genes can persist for years, even in an antibiotic-free environment. In this study, we investigated the potential of three fecal complex microbial communities from antibiotic-naive does to drive the microbiota of kits from antibiotic-exposed dams and outcompete bacteria-carrying antibiotic-resistant genes. The fecal complex microbial communities were either orally delivered or simply added as fresh fecal pellets in four to five nests that were kept clean from maternal feces. Additionally, four nests were cleaned for the maternal feces and five nests were handled according to the common farm practice (i.e., cleaning once a week) as controls. At weaning, we measured the relative abundance of 26 antibiotic resistance genes, the proportion of Enterobacteriaceae resistant to tetracycline and sulfonamide antibiotics, and the taxonomic composition of the microbiota by sequencing the 16S rRNA genes of one kit per nest. Changing the surrounding microbes of the kits can hinder the transmission of antibiotic resistance genes from one generation to the next, but the three communities widely differed in their ability to orient gut microbes and in their impact on antibiotic resistance genes. The most efficient delivery of the microbial community reduced the proportion of resistant Enterobacteria from 93 to 9%, decreased the relative abundance of eight antibiotic resistance genes, and changed the gut microbes of the kits at weaning. The least efficient did not reduce any ARG or modify the bacterial community. In addition, adding fecal pellets was more efficient than the oral inoculation of the anaerobic suspension derived from these fecal pellets. However, we were unable to predict the outcome of the exclusion from the data of the donor does (species composition and abundance of antibiotic resistance genes). In conclusion, we revealed major differences between microbial communities regarding their ability to exclude antibiotic resistance genes, but more work is needed to understand the components leading to the successful exclusion of antibiotic resistance genes from the gut. As a consequence, studies about the impact of competitive exclusion should use several microbial communities in order to draw general conclusions.
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spelling pubmed-66152582019-07-22 Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits Achard, Caroline Stéphanie Dupouy, Véronique Siviglia, Suzanne Arpaillange, Nathalie Cauquil, Laurent Bousquet-Mélou, Alain Zemb, Olivier Front Microbiol Microbiology Reducing antibiotic use is a necessary step toward less antibiotic resistance in livestock, but many antibiotic resistance genes can persist for years, even in an antibiotic-free environment. In this study, we investigated the potential of three fecal complex microbial communities from antibiotic-naive does to drive the microbiota of kits from antibiotic-exposed dams and outcompete bacteria-carrying antibiotic-resistant genes. The fecal complex microbial communities were either orally delivered or simply added as fresh fecal pellets in four to five nests that were kept clean from maternal feces. Additionally, four nests were cleaned for the maternal feces and five nests were handled according to the common farm practice (i.e., cleaning once a week) as controls. At weaning, we measured the relative abundance of 26 antibiotic resistance genes, the proportion of Enterobacteriaceae resistant to tetracycline and sulfonamide antibiotics, and the taxonomic composition of the microbiota by sequencing the 16S rRNA genes of one kit per nest. Changing the surrounding microbes of the kits can hinder the transmission of antibiotic resistance genes from one generation to the next, but the three communities widely differed in their ability to orient gut microbes and in their impact on antibiotic resistance genes. The most efficient delivery of the microbial community reduced the proportion of resistant Enterobacteria from 93 to 9%, decreased the relative abundance of eight antibiotic resistance genes, and changed the gut microbes of the kits at weaning. The least efficient did not reduce any ARG or modify the bacterial community. In addition, adding fecal pellets was more efficient than the oral inoculation of the anaerobic suspension derived from these fecal pellets. However, we were unable to predict the outcome of the exclusion from the data of the donor does (species composition and abundance of antibiotic resistance genes). In conclusion, we revealed major differences between microbial communities regarding their ability to exclude antibiotic resistance genes, but more work is needed to understand the components leading to the successful exclusion of antibiotic resistance genes from the gut. As a consequence, studies about the impact of competitive exclusion should use several microbial communities in order to draw general conclusions. Frontiers Media S.A. 2019-07-02 /pmc/articles/PMC6615258/ /pubmed/31333614 http://dx.doi.org/10.3389/fmicb.2019.01503 Text en Copyright © 2019 Achard, Dupouy, Siviglia, Arpaillange, Cauquil, Bousquet-Mélou and Zemb. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Achard, Caroline Stéphanie
Dupouy, Véronique
Siviglia, Suzanne
Arpaillange, Nathalie
Cauquil, Laurent
Bousquet-Mélou, Alain
Zemb, Olivier
Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits
title Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits
title_full Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits
title_fullStr Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits
title_full_unstemmed Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits
title_short Variability of the Ability of Complex Microbial Communities to Exclude Microbes Carrying Antibiotic Resistance Genes in Rabbits
title_sort variability of the ability of complex microbial communities to exclude microbes carrying antibiotic resistance genes in rabbits
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6615258/
https://www.ncbi.nlm.nih.gov/pubmed/31333614
http://dx.doi.org/10.3389/fmicb.2019.01503
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