Genome-resolved metagenomics of milk microbiomes reveals the influence of maternal dietary fiber on neonatal inheritance of immunoregulatory traits

AbstractBreastfeeding facilitates vertical transmission of microbes from mothers to infants. Milk microbiome composition is strongly influenced by maternal diet, and this affects which taxa are likely to colonize the infant gut with consequences for host health and immune development. At present, it is unclear how diet influences the composition of the milk microbiome and why these microbes lead to different health outcomes for the infant. Here, we used metagenomics and metabolomics to link microbially-mediated immunoregulatory traits and metabolites to individual milk microbial taxa, and determine how the representation of these traits changes with maternal dietary fiber content. We assembled and annotated genomes accounting for 90% of the milk microbial communities from breastfeeding mice fed high or low-fiber chow. Diverse carbohydrate and fatty acid content in high-fiber milk was associated with diverse microbes harboring multiple glycoside hydrolases and high redundancy of immunoregulatory metabolite pathways. Low dietary fiber, by contrast, produced milk enriched in amino acids and a low-diversity peptide degrading microbiome with limited immunoregulatory traits. Our study indicates that complex milk carbohydrate availability drives assembly of a diverse milk microbiome, and by extension a diverse set of immunoregulatory functions inheritable by the breastfeeding infant. Collectively, our findings highlight how the mother’s diet influences the composition of the milk microbiome and the potential vertical transmission of immunoregulatory traits from mother to infant.