Environmental remodeling of human gut microbiota and antibiotic resistome in livestock farms

Jian Sun,Alaric W D’Souza,José Luis Martínez,Ting Huang,Xian Bo Deng ,Bing Fang ,Xiaoping Liao ,Rong Min Zhang ,Yang Yu,You‐Zhi Tang ,Gautam Dantas,Sheng Hui Li ,Liang Li,Yong Xue Sun ,You Jun Feng ,Manish Boolchandani,Jiang Hong ,Zhi Wei Fang ,Yanyu Zhou ,Xin Lian ,Ke Cheng,Liang Xing Fang ,Qiu Long Yan ,Zhen Zeng ,Jing Xia,Ya Hong Liu

doi:10.1038/s41467-020-15222-y

Abstract

Anthropogenic environments have been implicated in enrichment and exchange of antibiotic resistance genes and bacteria. Here we study the impact of confined and controlled swine farm environments on temporal changes in the gut microbiome and resistome of veterinary students with occupational exposure for 3 months. By analyzing 16S rRNA and whole metagenome shotgun sequencing data in tandem with culture-based methods, we show that farm exposure shapes the gut microbiome of students, resulting in enrichment of potentially pathogenic taxa and antimicrobial resistance genes. Comparison of students’ gut microbiomes and resistomes to farm workers’ and environmental samples revealed extensive sharing of resistance genes and bacteria following exposure and after three months of their visit. Notably, antibiotic resistance genes were found in similar genetic contexts in student samples and farm environmental samples. Dynamic Bayesian network modeling predicted that the observed changes partially reverse over a 4-6 month period. Our results indicate that acute changes in a human’s living environment can persistently shape their gut microbiota and antibiotic resistome.

Highlights

Anthropogenic environments have been implicated in enrichment and exchange of antibiotic resistance genes and bacteria
To assess whether changes in the students’ gut microbiota and antibiotic resistome were correlated with their swine farm environmental contact, we examined the microbial landscape of the swine farm ecosystem via four representative environments: ventilation system dust, swine feces, sewage, and compost soil
We found an extensive network of antibiotic resistance (AR) gene sharing between microbial communities of humans and environments (Supplementary Fig. 12a, a similar network is found in ref. 20), and further revealed that 25% (477/1924) of AR genes detected in the students’ microbiota while on the farms co-localized with putative mobile genetic elements (MGEs), which are often involved in AR transfer across

Summary

Introduction

Anthropogenic environments have been implicated in enrichment and exchange of antibiotic resistance genes and bacteria. We performed 16S rRNA gene sequencing of 91 fecal samples collected longitudinally from 14 male student volunteers (at time points T0, T1–T3, and T4–T6; Fig. 1a), randomly assigned to different large-scale farms in China (Supplementary Fig. 1; Supplementary Data 1), to characterize temporal patterns in gut microbial community structure that occur with environmental changes.

Results

Conclusion