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 significant impact on public health, particularly in the context of increasing incidence of food-borne 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 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 (31% of variance 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 (>2.5?), 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.

人员高频流动的建成环境（如食品中心）内的微生物分布，可能对公共健康造成显著影响，在食源性暴发事件发生率持续上升的背景下尤为如此。在亚洲多座大型城市中，公共食品中心是民众就餐的主要场所，但目前我们对其环境微生物组（microbiome）仍缺乏基准认知。本研究针对新加坡16家公共食品中心开展了全市范围的宏基因组监测（metagenomic surveillance），共采集240份样本（n=240），旨在绘制两个时间节点下微生物（细菌、古菌、真菌、病毒）与非微生物DNA丰度的详细图谱。研究发现，相较于医院、办公室等其他环境，食品中心微生物组中富集了与食品相关的DNA特征序列，存在特定的食品-微生物关联（如肠杆菌科（Enterobacteriaceae）与鱼类），且食品DNA可部分解释观测到的微生物组特征（可解释31%的变异度）。机器学习分析筛选出22种微生物物种，可作为各食品中心高精度（准确率>80%）的位置特异性特征标志物，其中部分标志物在三年后仍可稳定存在。对抗生素抗性基因（antibiotic resistance genes, ARGs）与致病菌的分析显示，相较于其他非医疗环境，食品中心的ARGs富集程度令人意外（提升超2.5倍）；而相较于医院环境，其关键致病菌（如肺炎克雷伯菌（Klebsiella pneumoniae）、肠杆菌属（Enterobacter spp））的富集程度更是高出一个数量级。本研究结果表明，多种生物与非生物因素共同塑造了不同食品中心环境独特的微生物组特征，同时也证实了利用宏基因组监测来解析感染风险与抗生素抗性基因传播风险的应用潜力。