Metagenomic Assembly Reveals the Fate of the Core Antibiotic Resistome, its Hosts and Mobility in Animal Manure and After Compost

Background Antibiotics and antibiotic resistance genes (ARGs) used in intensive animal husbandry threaten human health worldwide; however, the core resistome, mobility of ARGs, and the composition of ARG hosts in animal manure and the following composts remain unclear. In the present study, metagenomic assembly was used to comprehensively decipher the core resistome and its potential mobility and hosts in animal manure and compost. Results In total, 201 ARGs were shared among different animal (layer, broiler, swine, beef cow, and dairy cow) manures and accounted for 86–99% of total relative abundance of ARGs, which mainly comprised multidrug, macrolide-lincosamide-streptogramin (M-L-S), tetracycline, beta-lactam, aminoglycoside, and sulfonamide resistance genes. Moreover, efficient composting reduced the total relative abundance of ARGs in manure from 0.938 to 0.405 copies per 16S rRNA gene; however, it did not have any remarkable effect on the multidrug, sulfonamide, and trimethoprim resistance genes. Procrustes analysis indicated that composting can reduce antibiotic residues and decrease the correlation between antibiotics and resistance genes. Furthermore, the ARG hosts included Proteobacteria (50.08%), Firmicutes (37.77%), Bacteroidetes (6.49%), and Actinobacteria (5.24%). In manure, aminoglycoside resistance genes were majorly found in Enterococcus, Streptococcus, and Enterobacter; tetracycline resistance genes (TRGs) were found in Pseudomonas, Lactobacillus, and Streptococcus; and multidrug resistance genes were mainly found in Escherichia coli. In our samples, ARGs were more prevalent in plasmids than in chromosomes. The broad host range and diverse mobile genetic elements may be two key factors for ARGs, such as sul1 and aadA, which could survive during composting. The multidrug resistance genes represented the dominant ARGs in pathogenic antibiotic-resistant bacteria (PARB) in manure, and composting could effectively control PARB. Conclusions Our experiments revealed the core resistome in animal manure, classified and relative quantified the ARG hosts, and assessed the mobility of ARGs. Composting can mitigate ARGs in animal manure by altering the bacterial hosts; however, some ARGs can escape from the removal with the survivor heat-tolerant hosts or transfer to these hosts. These findings will help optimize composting strategies for the effective treatment of ARGs and their hosts in farms.