Large-scale metagenomic analysis of food-associated microbial communities and their links with the human microbiome

Complex microbiomes are part of the food we eat: they are naturally present on the raw material, they merge along the food system, or they can be intentionally inoculated. Whether their presence is desired, such as in case of fermentation or probiotic supplementation, or undesired, in case of pathogenic or spoilage microbes, depends on who they are and what they are doing and therefore several studies investigated the microbiota of specific foods. However, the diversity of food microbiomes remains largely unexplored and similar studies present inconsistencies in methods and results. The study of the food microbiome is relevant also in light of the human microbiome and its multifaceted connection to hosts’ health status. Diet is one of the main factors influencing the human microbiome and many studies investigated how nutrition impacts the endogenous microbial communities both in the gut and in the oral cavity. Nevertheless, they largely overlooked the possibility of direct contribution of food-origin microorganisms. The primary aim of my PhD was the comprehensive characterization of foodborne microbial communities with the ultimate goal of estimating their impact on the human microbiome. This research intended to be humble contribution to the global effort in understanding the microbial sources building these composite ecosystems inhabiting the human body. In order to explore the food microbiome diversity, I selected and collected 583 publicly available food (shotgun) metagenomes and integrated them with 1950 newly sequenced food metagenomes. Through an assembly-based pipeline, I reconstructed >10,000 metagenome-assembled genomes (MAGs) that resulted in 290 previously undescribed taxa and, hence, firstly observed in this work. I characterized the composition of microbial communities in food, proving strong specificity across food categories and types through statistical analysis and machine learning approaches. The uniformly and coherently processed curated metadata, taxonomic profiles and reconstructed genomes are publicly available in a resource called curatedFoodMetagenomicData (cFMD). To investigate the presence of food-associated bacteria among human oral and gut microbiomes, I analyzed 20,000 human metagenomes available in curatedMetagenomicData (cMD) through the same expanded pipeline used for food samples. The overlap between food and human microbiomes showed high variations according to host characteristics and the food prevalent species accounted on average for 3% of relative abundance in adult microbiomes. I recognized 43 bacterial species prevalent in both environments that were investigated at the strain level, showing close genomic similarities of strains found both in food and humans.To our knowledge this was the first attempt to investigate the global food microbiome and to estimate its involvement in human microbiome at a large-scale. Our results showedan expansion of known and yet-to-be-isolated species associated with food microbiomes, their characterization to uncover microbial diversity and provide insights on links with the human microbiome, and the release of a publicly-available resource as cFMD that will support the use of metagenomics in food microbiology and food safety, certificationand quality control applications.