Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture

ABSTRACT Antibiotic resistance is a worldwide health risk, but the influence of animal agriculture on the genetic context and enrichment of individual antibiotic resistance alleles remains unclear. Using quantitative PCR followed by amplicon sequencing, we quantified and sequenced 44 genes related...

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Autores principales:	Timothy A. Johnson, Robert D. Stedtfeld, Qiong Wang, James R. Cole, Syed A. Hashsham, Torey Looft, Yong-Guan Zhu, James M. Tiedje
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/da146d2462a2499c915133b7b9a42bed
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spelling	oai:doaj.org-article:da146d2462a2499c915133b7b9a42bed2021-11-15T15:41:41ZClusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture10.1128/mBio.02214-152150-7511https://doaj.org/article/da146d2462a2499c915133b7b9a42bed2016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02214-15https://doaj.org/toc/2150-7511ABSTRACT Antibiotic resistance is a worldwide health risk, but the influence of animal agriculture on the genetic context and enrichment of individual antibiotic resistance alleles remains unclear. Using quantitative PCR followed by amplicon sequencing, we quantified and sequenced 44 genes related to antibiotic resistance, mobile genetic elements, and bacterial phylogeny in microbiomes from U.S. laboratory swine and from swine farms from three Chinese regions. We identified highly abundant resistance clusters: groups of resistance and mobile genetic element alleles that cooccur. For example, the abundance of genes conferring resistance to six classes of antibiotics together with class 1 integrase and the abundance of IS6100-type transposons in three Chinese regions are directly correlated. These resistance cluster genes likely colocalize in microbial genomes in the farms. Resistance cluster alleles were dramatically enriched (up to 1 to 10% as abundant as 16S rRNA) and indicate that multidrug-resistant bacteria are likely the norm rather than an exception in these communities. This enrichment largely occurred independently of phylogenetic composition; thus, resistance clusters are likely present in many bacterial taxa. Furthermore, resistance clusters contain resistance genes that confer resistance to antibiotics independently of their particular use on the farms. Selection for these clusters is likely due to the use of only a subset of the broad range of chemicals to which the clusters confer resistance. The scale of animal agriculture and its wastes, the enrichment and horizontal gene transfer potential of the clusters, and the vicinity of large human populations suggest that managing this resistance reservoir is important for minimizing human risk. IMPORTANCE Agricultural antibiotic use results in clusters of cooccurring resistance genes that together confer resistance to multiple antibiotics. The use of a single antibiotic could select for an entire suite of resistance genes if they are genetically linked. No links to bacterial membership were observed for these clusters of resistance genes. These findings urge deeper understanding of colocalization of resistance genes and mobile genetic elements in resistance islands and their distribution throughout antibiotic-exposed microbiomes. As governments seek to combat the rise in antibiotic resistance, a balance is sought between ensuring proper animal health and welfare and preserving medically important antibiotics for therapeutic use. Metagenomic and genomic monitoring will be critical to determine if resistance genes can be reduced in animal microbiomes, or if these gene clusters will continue to be coselected by antibiotics not deemed medically important for human health but used for growth promotion or by medically important antibiotics used therapeutically.Timothy A. JohnsonRobert D. StedtfeldQiong WangJames R. ColeSyed A. HashshamTorey LooftYong-Guan ZhuJames M. TiedjeAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Timothy A. Johnson Robert D. Stedtfeld Qiong Wang James R. Cole Syed A. Hashsham Torey Looft Yong-Guan Zhu James M. Tiedje Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
description	ABSTRACT Antibiotic resistance is a worldwide health risk, but the influence of animal agriculture on the genetic context and enrichment of individual antibiotic resistance alleles remains unclear. Using quantitative PCR followed by amplicon sequencing, we quantified and sequenced 44 genes related to antibiotic resistance, mobile genetic elements, and bacterial phylogeny in microbiomes from U.S. laboratory swine and from swine farms from three Chinese regions. We identified highly abundant resistance clusters: groups of resistance and mobile genetic element alleles that cooccur. For example, the abundance of genes conferring resistance to six classes of antibiotics together with class 1 integrase and the abundance of IS6100-type transposons in three Chinese regions are directly correlated. These resistance cluster genes likely colocalize in microbial genomes in the farms. Resistance cluster alleles were dramatically enriched (up to 1 to 10% as abundant as 16S rRNA) and indicate that multidrug-resistant bacteria are likely the norm rather than an exception in these communities. This enrichment largely occurred independently of phylogenetic composition; thus, resistance clusters are likely present in many bacterial taxa. Furthermore, resistance clusters contain resistance genes that confer resistance to antibiotics independently of their particular use on the farms. Selection for these clusters is likely due to the use of only a subset of the broad range of chemicals to which the clusters confer resistance. The scale of animal agriculture and its wastes, the enrichment and horizontal gene transfer potential of the clusters, and the vicinity of large human populations suggest that managing this resistance reservoir is important for minimizing human risk. IMPORTANCE Agricultural antibiotic use results in clusters of cooccurring resistance genes that together confer resistance to multiple antibiotics. The use of a single antibiotic could select for an entire suite of resistance genes if they are genetically linked. No links to bacterial membership were observed for these clusters of resistance genes. These findings urge deeper understanding of colocalization of resistance genes and mobile genetic elements in resistance islands and their distribution throughout antibiotic-exposed microbiomes. As governments seek to combat the rise in antibiotic resistance, a balance is sought between ensuring proper animal health and welfare and preserving medically important antibiotics for therapeutic use. Metagenomic and genomic monitoring will be critical to determine if resistance genes can be reduced in animal microbiomes, or if these gene clusters will continue to be coselected by antibiotics not deemed medically important for human health but used for growth promotion or by medically important antibiotics used therapeutically.
format	article
author	Timothy A. Johnson Robert D. Stedtfeld Qiong Wang James R. Cole Syed A. Hashsham Torey Looft Yong-Guan Zhu James M. Tiedje
author_facet	Timothy A. Johnson Robert D. Stedtfeld Qiong Wang James R. Cole Syed A. Hashsham Torey Looft Yong-Guan Zhu James M. Tiedje
author_sort	Timothy A. Johnson
title	Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
title_short	Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
title_full	Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
title_fullStr	Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
title_full_unstemmed	Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
title_sort	clusters of antibiotic resistance genes enriched together stay together in swine agriculture
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/da146d2462a2499c915133b7b9a42bed
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Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture

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