Correlation of microbiota and antibiotic resistance genes in the swine manure-soil interface in Chongming Island

Abstract

Abstract Background: Swine farming is a widespread agricultural practice that produces a substantial amount of antibiotics and genes associated with antibiotic resistance in swine manure. The presence of these antibiotic resistance genes (ARGs) poses a potential threat to the environment and human health. In order to investigate the microbiota and ARG profiles of swine manure and soil, samples from five swine farms on Chongming Island were collected and high-throughput sequencing and bioinformatics analysis were conducted. The sequencing data and MetaCompare allowed us to estimate the risk of ARG transmission to human pathogens in the sampled environments and prioritize the potential for antibiotic resistance.Results: Significant differences in microbial communities and antibiotic resistance gene (ARG) profiles were revealed both in swine manure and soil samples from five farms. Bacteroidetes was the dominant phylum in swine manure, while Proteobacteria was dominant in soil. The abundance of different drug classes varied from manure to soil. Multidrug, tetracycline, glycopeptide, peptide, fluoroquinolone, beta-lactam, rifamycin, macrolide, and aminoglycoside were the main drug classes of ARGs identified in both samples, with a large proportion of macrolide-lincosamide-streptogramin (MLS) and carbapenem resistance genes. Samples from the same farm showed a strong correlation in microbiota abundance and resistance gene diversity, indicating the effect of swine manure application and composting on the soil. However, microbial communities and ARGs varied among samples collected from different farms, influenced by factors including but not limited to feed composition, feeding density, husbandry practices, and sanitation. Beneficial bacteria in swine manure, including Bacillus spp., Eubacterium spp., Lactobacillus spp., Blautia, Dorea, and Methanobrevibacter, had symbiotic relationships with one another at the pig manure-soil interface. These genera were able to inhibit the growth of opportunistic pathogenic bacteria, such as Escherichia spp. However, some beneficial bacteria, represented by the NmcR gene, may promote the spread of antimicrobial resistance. We also observed numerous symbiotic relationships between different species of drug resistance genes, including cdeA, Bbif_ileS_MUP, macB, patB, vanSD, and tetQ, among others. Microbiota were found to determine the composition of drug resistance gene profiles. Quantifying the health risks associated with antibiotic resistance can help us identify and mitigate the risk. The mean risk value of ARGs for swine manure and soil samples from the five farms was 23.42 and 22.23 respectively, with higher values indicating greater risk.Conclusion Our study sheds light on the complex relationships between microbiota and ARG profiles in swine manure and soil, and highlights the potential impact of swine farming practices on the environment and public health.