National Food Institute, Technical University of Denmark, Lyngby, Denmark.
Institute for Risk Assessment Sciences, Faculty of Veterinary Medicine, Utrecht University, The Netherlands, Utrecht.
mSystems. 2024 Apr 16;9(4):e0132823. doi: 10.1128/msystems.01328-23. Epub 2024 Mar 19.
Metagenomic sequencing has proven to be a powerful tool in the monitoring of antimicrobial resistance (AMR). Here, we provide a comparative analysis of the resistome from pigs, poultry, veal calves, turkey, and rainbow trout, for a total of 538 herds across nine European countries. We calculated the effects of per-farm management practices and antimicrobial usage (AMU) on the resistome in pigs, broilers, and veal calves. We also provide an in-depth study of the associations between bacterial diversity, resistome diversity, and AMR abundances as well as co-occurrence analysis of bacterial taxa and antimicrobial resistance genes (ARGs) and the universality of the latter. The resistomes of veal calves and pigs clustered together, as did those of avian origin, while the rainbow trout resistome was different. Moreover, we identified clear core resistomes for each specific food-producing animal species. We identified positive associations between bacterial alpha diversity and both resistome alpha diversity and abundance. Network analyses revealed very few taxa-ARG associations in pigs but a large number for the avian species. Using updated reference databases and optimized bioinformatics, previously reported significant associations between AMU, biosecurity, and AMR in pig and poultry farms were validated. AMU is an important driver for AMR; however, our integrated analyses suggest that factors contributing to increased bacterial diversity might also be associated with higher AMR load. We also found that dispersal limitations of ARGs are shaping livestock resistomes, and future efforts to fight AMR should continue to emphasize biosecurity measures.IMPORTANCEUnderstanding the occurrence, diversity, and drivers for antimicrobial resistance (AMR) is important to focus future control efforts. So far, almost all attempts to limit AMR in livestock have addressed antimicrobial consumption. We here performed an integrated analysis of the resistomes of five important farmed animal populations across Europe finding that the resistome and AMR levels are also shaped by factors related to bacterial diversity, as well as dispersal limitations. Thus, future studies and interventions aimed at reducing AMR should not only address antimicrobial usage but also consider other epidemiological and ecological factors.
宏基因组测序已被证明是监测抗生素耐药性（AMR）的有力工具。在这里，我们对来自猪、家禽、小牛肉牛、火鸡和虹鳟鱼的耐药组进行了比较分析，总共涉及 9 个欧洲国家的 538 个畜群。我们计算了每个农场管理实践和抗生素使用（AMU）对猪、肉鸡和小牛肉牛耐药组的影响。我们还深入研究了细菌多样性、耐药组多样性与 AMR 丰度之间的关联，以及细菌分类群和抗生素耐药基因（ARGs）的共存分析，以及后者的普遍性。小牛肉牛和猪的耐药组与禽类起源的耐药组聚集在一起，而虹鳟鱼的耐药组则不同。此外，我们确定了每个特定食用动物物种的明确核心耐药组。我们发现细菌α多样性与耐药组α多样性和丰度之间存在正相关。网络分析表明，猪只中很少有类群-ARGs 关联，但禽类中有大量的类群-ARGs 关联。使用更新的参考数据库和优化的生物信息学，验证了先前报道的猪和家禽养殖场中 AMU、生物安全和 AMR 之间的显著关联。AMU 是 AMR 的重要驱动因素；然而，我们的综合分析表明，导致细菌多样性增加的因素也可能与更高的 AMR 负荷有关。我们还发现，ARGs 的扩散限制正在塑造家畜耐药组，未来对抗 AMR 的努力应继续强调生物安全措施。
重要性
了解抗生素耐药性（AMR）的发生、多样性和驱动因素对于集中未来的控制工作非常重要。到目前为止，几乎所有限制牲畜 AMR 的尝试都解决了抗生素的消耗问题。在这里，我们对欧洲五个重要养殖动物种群的耐药组进行了综合分析，发现耐药组和 AMR 水平也受到与细菌多样性以及扩散限制相关的因素的影响。因此，未来旨在减少 AMR 的研究和干预措施不仅应解决抗生素使用问题，还应考虑其他流行病学和生态学因素。
