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

Héctor Puente,Fiona Crispie,Oscar Mencía-Ares,Raúl Cabrera-Rubio,Pedro Rubio,José Francisco Cobo-Díaz,Ana Carvajal,Paul D. Cotter,Héctor Argüello,Manuel Gómez-García,Avelino Álvarez-Ordóñez

doi:10.1186/s40168-020-00941-7

Abstract

BackgroundThe 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.ResultsOur 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.ConclusionsOverall, this study shows how AMU, production system, and sample type influence, mainly through MGEs, the profile and dispersion of ARGs in pig production.-mkotjguAeV5vmuT7Jtr8vVideo

Highlights

The global threat of antimicrobial resistance (AMR) is a One Health problem impacted by antimicrobial use (AMU) for human and livestock applications
Inverse Simpson and Antimicrobial resistance gene (ARG) richness indexes showed that the total ARGs diversity was significantly lower in feces, both from intensive and extensive farms, than in farm environments and slurry samples
A higher ARG abundance was observed in samples recovered from intensive swine farms, with higher Antimicrobial use (AMU), relative to those from extensive herds

Summary

Introduction

The global threat of antimicrobial resistance (AMR) is a One Health problem impacted by antimicrobial use (AMU) for human and livestock applications. Antimicrobial resistance (AMR) is one of the largest threats to global health and food security [1, 2]. Antimicrobial use (AMU) in human medicine is an important factor, but it is widely recognized that the use of antimicrobials in food-producing animals contributes to the burden of AMR in human health [3]. Monitoring of indicator and zoonotic bacteria on pig farms reveals a frequent detection of AMR [9] and the presence of certain antimicrobial resistance genes (ARGs) of critical importance, such as blaCTX-M, mecA, or mcr [10,11,12]. Metagenomic approaches complement traditional AMR surveillance systems by characterizing the total pool of ARGs, including those on mobile genetic elements (MGEs), in the whole microbial community [13,14,15]

Methods

Results

Discussion

Conclusion