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Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes

BACKGROUND: Antimicrobial agents have been widely used in animal farms to prevent and treat animal diseases and to promote growth. Antimicrobial agents may change the bacterial community and enhance the resistome in animal feces. We used metagenome-wide analysis to investigate the changes in bacteri...

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Autores principales: Xiong, Wenguang, Wang, Yulin, Sun, Yongxue, Ma, Liping, Zeng, Qinglin, Jiang, Xiaotao, Li, Andong, Zeng, Zhenling, Zhang, Tong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5811963/
https://www.ncbi.nlm.nih.gov/pubmed/29439741
http://dx.doi.org/10.1186/s40168-018-0419-2
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author Xiong, Wenguang
Wang, Yulin
Sun, Yongxue
Ma, Liping
Zeng, Qinglin
Jiang, Xiaotao
Li, Andong
Zeng, Zhenling
Zhang, Tong
author_facet Xiong, Wenguang
Wang, Yulin
Sun, Yongxue
Ma, Liping
Zeng, Qinglin
Jiang, Xiaotao
Li, Andong
Zeng, Zhenling
Zhang, Tong
author_sort Xiong, Wenguang
collection PubMed
description BACKGROUND: Antimicrobial agents have been widely used in animal farms to prevent and treat animal diseases and to promote growth. Antimicrobial agents may change the bacterial community and enhance the resistome in animal feces. We used metagenome-wide analysis to investigate the changes in bacterial community, variations in antibiotic resistance genes (ARGs), and their bacterial hosts in the feces of broiler chickens over a full-treatment course of chlortetracycline at low and therapeutic dose levels. RESULTS: The effects of chlortetracycline on resistome were dependent on the specific ARG subtypes and not simply the overall community-level ARGs. Therapeutic dose of chlortetracycline promoted the abundance of tetracycline resistance genes (tetA and tetW) and inhibited multidrug resistance genes (mdtA, mdtC, mdtK, ompR, and TolC). The therapeutic dose of chlortetracycline led to loss of Proteobacteria mainly due to the decrease of Escherichia/Shigella (from 72 to 58%). Inhibition of Escherichia by chlortetracycline was the primary reason for the decrease of genes resistant to multiple drugs in the therapeutic dose group. The ARG host Bifidobacterium were enriched due to tetW harbored by Bifidobacterium under chlortetracycline treatment. Escherichia was always the major host for multidrug resistance genes, whereas the primary host was changed from Escherichia to Klebsiella for aminoglycoside resistance genes with the treatment of therapeutic dose of chlortetracycline. CONCLUSIONS: We provided the first metagenomic insights into antibiotic-mediated alteration of ARG-harboring bacterial hosts at community-wide level in chicken feces. These results indicated that the changes in the structure of antibiotic-induced feces microbial communities accompany changes in the abundance of bacterial hosts carrying specific ARGs in the feces microbiota. These findings will help to optimize therapeutic schemes for the effective treatment of antibiotic resistant pathogens in poultry farms. GRAPHICAL ABSTRACT: Resistome variations in faecal microbiome of chickens exposed to chlortetracycline [Image: see text] ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0419-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-58119632018-02-15 Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes Xiong, Wenguang Wang, Yulin Sun, Yongxue Ma, Liping Zeng, Qinglin Jiang, Xiaotao Li, Andong Zeng, Zhenling Zhang, Tong Microbiome Research BACKGROUND: Antimicrobial agents have been widely used in animal farms to prevent and treat animal diseases and to promote growth. Antimicrobial agents may change the bacterial community and enhance the resistome in animal feces. We used metagenome-wide analysis to investigate the changes in bacterial community, variations in antibiotic resistance genes (ARGs), and their bacterial hosts in the feces of broiler chickens over a full-treatment course of chlortetracycline at low and therapeutic dose levels. RESULTS: The effects of chlortetracycline on resistome were dependent on the specific ARG subtypes and not simply the overall community-level ARGs. Therapeutic dose of chlortetracycline promoted the abundance of tetracycline resistance genes (tetA and tetW) and inhibited multidrug resistance genes (mdtA, mdtC, mdtK, ompR, and TolC). The therapeutic dose of chlortetracycline led to loss of Proteobacteria mainly due to the decrease of Escherichia/Shigella (from 72 to 58%). Inhibition of Escherichia by chlortetracycline was the primary reason for the decrease of genes resistant to multiple drugs in the therapeutic dose group. The ARG host Bifidobacterium were enriched due to tetW harbored by Bifidobacterium under chlortetracycline treatment. Escherichia was always the major host for multidrug resistance genes, whereas the primary host was changed from Escherichia to Klebsiella for aminoglycoside resistance genes with the treatment of therapeutic dose of chlortetracycline. CONCLUSIONS: We provided the first metagenomic insights into antibiotic-mediated alteration of ARG-harboring bacterial hosts at community-wide level in chicken feces. These results indicated that the changes in the structure of antibiotic-induced feces microbial communities accompany changes in the abundance of bacterial hosts carrying specific ARGs in the feces microbiota. These findings will help to optimize therapeutic schemes for the effective treatment of antibiotic resistant pathogens in poultry farms. GRAPHICAL ABSTRACT: Resistome variations in faecal microbiome of chickens exposed to chlortetracycline [Image: see text] ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0419-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-02-13 /pmc/articles/PMC5811963/ /pubmed/29439741 http://dx.doi.org/10.1186/s40168-018-0419-2 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Xiong, Wenguang
Wang, Yulin
Sun, Yongxue
Ma, Liping
Zeng, Qinglin
Jiang, Xiaotao
Li, Andong
Zeng, Zhenling
Zhang, Tong
Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes
title Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes
title_full Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes
title_fullStr Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes
title_full_unstemmed Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes
title_short Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes
title_sort antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5811963/
https://www.ncbi.nlm.nih.gov/pubmed/29439741
http://dx.doi.org/10.1186/s40168-018-0419-2
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