Straw-based compost cultivation disproportionally contributes to the environmental persistence of antibiotic resistance from raw cattle manure to organic vegetables

Abstract

Cattle manure, is a reservoir of antimicrobial resistance genes, but the mechanisms by which they migrate from farm to table remain obscure. Here, we chose Agaricus bisporus as a model vegetable to examine such migration and characterized the resistome in 112 metagenomes covering samples from raw manure, composting substrates, rhizosphere, and surfaces of mushrooms. A total of 1864 resistance genes, representing 113 unique mechanisms of resistance, were identified. Monensin treatment on beef specifically enriched fecal resistance genes within Moraxellaceae, but this effect did not persist in downstream mushrooms. Interestingly, we found that resistance genes were significantly more enriched on mushroom surfaces when cultivated with corn-based compost compared to rice and wheat, likely a result of the disproportional propagation of Pseudomonadaceae and varied ability of lateral gene transfer. Importantly, our sequence alignment together with genome-centric analysis observed that 89 resistance genes, mainly conferring resistance to drug and biocide (20.22%) and mercury (19.10%), were shared across all types of samples, indicating an efficient transmission of resistance in food production. Moreover, co-occurrence of genes conferring resistance to different compounds frequently occurred in parallel with microbial migration. Together, we present the influences of antibiotic treatment and straw-based composting on resistome along the mushroom production chain (from manure to straw-based compost, rhizosphere of compost cultivated mushroom and surface of mushroom) and highlighted the risks of resistance genes migration.