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The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs

Antibiotics are widely used in pig farming across the world which has led to concerns about the potential impact on human health through the selection of antibiotic resistant pathogenic bacteria. This worry has resulted in the development of a production scheme known as pigs Raised Without Antibioti...

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Autores principales: Tams, Katrine Wegener, Larsen, Inge, Hansen, Julie Elvekjær, Spiegelhauer, Henrik, Strøm-Hansen, Alexander Damm, Rasmussen, Sophia, Ingham, Anna Cäcilia, Kalmar, Lajos, Kean, Iain Robert Louis, Angen, Øystein, Holmes, Mark A., Pedersen, Karl, Jelsbak, Lars, Folkesson, Anders, Larsen, Anders Rhod, Strube, Mikael Lenz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10440943/
https://www.ncbi.nlm.nih.gov/pubmed/37605221
http://dx.doi.org/10.1186/s42523-023-00258-4
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author Tams, Katrine Wegener
Larsen, Inge
Hansen, Julie Elvekjær
Spiegelhauer, Henrik
Strøm-Hansen, Alexander Damm
Rasmussen, Sophia
Ingham, Anna Cäcilia
Kalmar, Lajos
Kean, Iain Robert Louis
Angen, Øystein
Holmes, Mark A.
Pedersen, Karl
Jelsbak, Lars
Folkesson, Anders
Larsen, Anders Rhod
Strube, Mikael Lenz
author_facet Tams, Katrine Wegener
Larsen, Inge
Hansen, Julie Elvekjær
Spiegelhauer, Henrik
Strøm-Hansen, Alexander Damm
Rasmussen, Sophia
Ingham, Anna Cäcilia
Kalmar, Lajos
Kean, Iain Robert Louis
Angen, Øystein
Holmes, Mark A.
Pedersen, Karl
Jelsbak, Lars
Folkesson, Anders
Larsen, Anders Rhod
Strube, Mikael Lenz
author_sort Tams, Katrine Wegener
collection PubMed
description Antibiotics are widely used in pig farming across the world which has led to concerns about the potential impact on human health through the selection of antibiotic resistant pathogenic bacteria. This worry has resulted in the development of a production scheme known as pigs Raised Without Antibiotics (RWA), in which pigs are produced in commercial farms, but are ear-tagged as RWA until slaughter unless they receive treatment, thus allowing the farmer to sell the pigs either as premium priced RWA or as conventional meat. Development of antibiotic resistance in pig farming has been studied in national surveys of antibiotic usage and resistance, as well as in experimental studies of groups of pigs, but not in individual pigs followed longitudinally in a commercial pig farm. In this study, a cohort of RWA designated pigs were sampled at 10 time points from birth until slaughter along with pen-mates treated with antibiotics at the same farm. From these samples, the microbiome, determined using 16S sequencing, and the resistome, as determined using qPCR for 82 resistance genes, was investigated, allowing us to examine the difference between RWA pigs and antibiotic treated pigs. We furthermore included 176 additional pigs from six different RWA farms which were sampled at the slaughterhouse as an endpoint to substantiate the cohort as well as for evaluation of intra-farm variability. The results showed a clear effect of age in both the microbiome and resistome composition from early life up until slaughter. As a function of antibiotic treatment, however, we observed a small but significant divergence between treated and untreated animals in their microbiome composition immediately following treatment, which disappeared before 8 weeks of age. The effect on the resistome was evident and an effect of treatment could still be detected at week 8. In animals sampled at the slaughterhouse, we observed no difference in the microbiome or the resistome as a result of treatment status but did see a strong effect of farm origin. Network analysis of co-occurrence of microbiome and resistome data suggested that some resistance genes may be transferred through mobile genetic elements, so we used Hi-C metagenomics on a subset of samples to investigate this. We conclude that antibiotic treatment has a differential effect on the microbiome vs. the resistome and that although resistance gene load is increased by antibiotic treatment load, this effect disappears before slaughter. More studies are needed to elucidate the optimal way to rear pigs without antibiotics. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00258-4.
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spelling pubmed-104409432023-08-22 The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs Tams, Katrine Wegener Larsen, Inge Hansen, Julie Elvekjær Spiegelhauer, Henrik Strøm-Hansen, Alexander Damm Rasmussen, Sophia Ingham, Anna Cäcilia Kalmar, Lajos Kean, Iain Robert Louis Angen, Øystein Holmes, Mark A. Pedersen, Karl Jelsbak, Lars Folkesson, Anders Larsen, Anders Rhod Strube, Mikael Lenz Anim Microbiome Research Antibiotics are widely used in pig farming across the world which has led to concerns about the potential impact on human health through the selection of antibiotic resistant pathogenic bacteria. This worry has resulted in the development of a production scheme known as pigs Raised Without Antibiotics (RWA), in which pigs are produced in commercial farms, but are ear-tagged as RWA until slaughter unless they receive treatment, thus allowing the farmer to sell the pigs either as premium priced RWA or as conventional meat. Development of antibiotic resistance in pig farming has been studied in national surveys of antibiotic usage and resistance, as well as in experimental studies of groups of pigs, but not in individual pigs followed longitudinally in a commercial pig farm. In this study, a cohort of RWA designated pigs were sampled at 10 time points from birth until slaughter along with pen-mates treated with antibiotics at the same farm. From these samples, the microbiome, determined using 16S sequencing, and the resistome, as determined using qPCR for 82 resistance genes, was investigated, allowing us to examine the difference between RWA pigs and antibiotic treated pigs. We furthermore included 176 additional pigs from six different RWA farms which were sampled at the slaughterhouse as an endpoint to substantiate the cohort as well as for evaluation of intra-farm variability. The results showed a clear effect of age in both the microbiome and resistome composition from early life up until slaughter. As a function of antibiotic treatment, however, we observed a small but significant divergence between treated and untreated animals in their microbiome composition immediately following treatment, which disappeared before 8 weeks of age. The effect on the resistome was evident and an effect of treatment could still be detected at week 8. In animals sampled at the slaughterhouse, we observed no difference in the microbiome or the resistome as a result of treatment status but did see a strong effect of farm origin. Network analysis of co-occurrence of microbiome and resistome data suggested that some resistance genes may be transferred through mobile genetic elements, so we used Hi-C metagenomics on a subset of samples to investigate this. We conclude that antibiotic treatment has a differential effect on the microbiome vs. the resistome and that although resistance gene load is increased by antibiotic treatment load, this effect disappears before slaughter. More studies are needed to elucidate the optimal way to rear pigs without antibiotics. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00258-4. BioMed Central 2023-08-21 /pmc/articles/PMC10440943/ /pubmed/37605221 http://dx.doi.org/10.1186/s42523-023-00258-4 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 Research
Tams, Katrine Wegener
Larsen, Inge
Hansen, Julie Elvekjær
Spiegelhauer, Henrik
Strøm-Hansen, Alexander Damm
Rasmussen, Sophia
Ingham, Anna Cäcilia
Kalmar, Lajos
Kean, Iain Robert Louis
Angen, Øystein
Holmes, Mark A.
Pedersen, Karl
Jelsbak, Lars
Folkesson, Anders
Larsen, Anders Rhod
Strube, Mikael Lenz
The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs
title The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs
title_full The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs
title_fullStr The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs
title_full_unstemmed The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs
title_short The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs
title_sort effects of antibiotic use on the dynamics of the microbiome and resistome in pigs
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10440943/
https://www.ncbi.nlm.nih.gov/pubmed/37605221
http://dx.doi.org/10.1186/s42523-023-00258-4
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