City-wide metagenomic surveillance of food centres reveals location-specific microbial signatures and enrichment of antibiotic resistance genes

The distribution of microorganisms in built environments with high human traffic, such as food centres, can potentially have a significant impact on public health, particularly in the context of increasing worldwide incidence of food and fomite-related outbreaks. In several major Asian cities, public food centres are the main venue for food consumption and yet we lack a baseline understanding of their environmental microbiomes. We conducted city-wide metagenomic surveillance of food-centre microbiomes in Singapore (16 centres, n=240 samples) to provide a detailed map of microbial (bacteria, archaea, fungi, viruses) as well as non-microbial DNA abundances across two timepoints. Food-centre microbiomes were found to be enriched in food-related DNA signatures compared to other environments such as hospitals and offices, with specific food-microbe associations (e.g. Enterobacteriaceae and fish) and food DNA providing a partial explanation for the microbial profiles observed (44% of variation explained). Machine learning analysis identified a small set of microbial species (n=22) that serve as highly accurate (>80%) location-specific signatures for various food centres, some of which persist even after 3 years. Profiling of antibiotic resistance genes (ARGs) and pathogens identified a surprising enrichment of ARGs in food centres relative to other non-healthcare environments (>2.5x;), and an order of magnitude enrichment of key pathogenic species (e.g. Klebsiella pneumoniae, Enterobacter spp) even compared to hospital environments. These results highlight the contribution of diverse biotic and abiotic factors in shaping the unique microbiome profiles of different food-centre environments, and the potential for using metagenomic surveillance to understand the risk for infections and antibiotic resistance gene transmission.