Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms

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Date
2020
Authors
Mencía-Ares, Oscar
Cabrera-Rubio, Raúl
Cobo-Díaz, José Francisco
Álvarez-Ordóñez, Avelino
Gómez-García, Manuel
Puente, Héctor
Cotter, Paul D.
Crispie, Fiona
Carvajal, Ana
Rubio, Pedro
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BioMed Central Ltd
Published Version
10.1186/s40168-020-00941-7
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Abstract
Background: The global threat of antimicrobial resistance (AMR) is a One Health problem impacted by antimicrobial use (AMU) for human and livestock applications. Extensive Iberian swine production is based on a more sustainable and eco-friendly management system, providing an excellent opportunity to evaluate how sustained differences in AMU impact the resistome, not only in the animals but also on the farm environment. Here, we evaluate the resistome footprint of an extensive pig farming system, maintained for decades, as compared to that of industrialized intensive pig farming by analyzing 105 fecal, environmental and slurry metagenomes from 38 farms. Results: Our results evidence a significantly higher abundance of antimicrobial resistance genes (ARGs) on intensive farms and a link between AMU and AMR to certain antimicrobial classes. We observed differences in the resistome across sample types, with a higher richness and dispersion of ARGs within environmental samples than on those from feces or slurry. Indeed, a deeper analysis revealed that differences among the three sample types were defined by taxa-ARGs associations. Interestingly, mobilome analyses revealed that the observed AMR differences between intensive and extensive farms could be linked to differences in the abundance of mobile genetic elements (MGEs). Thus, while there were no differences in the abundance of chromosomal-associated ARGs between intensive and extensive herds, a significantly higher abundance of integrons in the environment and plasmids, regardless of the sample type, was detected on intensive farms. Conclusions: Overall, this study shows how AMU, production system, and sample type influence, mainly through MGEs, the profile and dispersion of ARGs in pig production.
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Keywords
Antimicrobial resistance , Farm environment , Feces , Mobilome , One health , Sustainable farming , Swine
Citation
Mencía-Ares, O., Cabrera-Rubio, R., Cobo-Díaz, J.F., Álvarez-Ordóñez, A., Gómez-García, M., Puente, H., Cotter, P.D., Crispie, F., Carvajal, A., Rubio, P. and Argüello, H. (2020) ‘Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms’, Microbiome, 8(1), 164 (17pp). doi: 10.1186/s40168-020-00941-7
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https://hdl.handle.net/10468/13557
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APC Microbiome Ireland - Journal Articles
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© 2020, the Authors. 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/. 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 in a credit line to the data.