Uncovering the resistome and mobilome across different types of ready-to-eat fermented foods

Abstract

Antimicrobial resistance in food poses a significant threat to public health, and the persistence of antibiotic resistance genes (ARGs) in ready-to-eat fermented foods (RTE-FFs) is a growing concern. However, information on the diversity, origins, and transferability of ARGs in RTE-FFs is limited. This study investigated the distribution of ARGs and mobile genetic elements (MGEs) in four types of RTE-FFs: soybean, dairy, meat, and vegetable products. Using whole metagenomic sequencing, we identified significant variations in the bacterial diversity, ARG profiles, and MGE profiles among these food types. Bean-based RTE-FFs exhibited the highest diversity of ARGs and MGEs, while dairy products showed the lowest diversity (p < 0.05). Eight types of ARGs were significantly more prevalent in bean-based foods than in the other food categories (p < 0.05). Several ARGs were highly abundant in the RTE-FFs, including aphA2, blaTEM-116, PBP1a, PBP1b, OqxA, OqxBgb, lsa(A), tet(34), and tet(58). Plasmids carried the highest number of ARGs among all MGEs, particularly those associated with beta-lactam, macrolide-lincosamide-streptogramin, tetracycline, and aminoglycoside resistance, suggesting a higher risk with plasmid-mediated transfer, especially in bean-based RTE-FFs. Metagenomic binning analysis recovered 76 high-quality metagenome-assembled genomes (MAGs), including four novel species. A total of 13 types of ARGs, encompassing 95 subtypes, were identified across the MAGs; Bacillus paranthracis, Enterococcus casseliflavus, and Enterococcus gallinarum had the most ARGs (16, 12, and 14, respectively). Dairy RTE-FFs (yogurt and cheese) contained a high abundance of Streptococcus thermophilus resistant to beta-lactams (PBP1b) and tetracycline (tetB(60)), raising concerns about ARG transfer in these food products. Bean RTE-FFs (sufu) harbored two pathogenic Acinetobacter species carrying carbapenem resistance genes (blaOXA-180, blaOXA-211, and blaOXA-230). No ARGs were found in the MGEs (prophages, insertion sequences, or transposons) within the MAGs. Overall, our results provide valuable insights into the antibiotic resistome and mobilome of various RTE-FFs to inform food production and management practices.

Keywords: Antibiotic resistance genes; Horizontal gene transfer; Metagenome-assembled genomes; Metagenomics; Mobile genetic elements; Ready-to-eat fermented foods.