Selective maternal seeding and environment shape the human gut microbiome

Vertical transmission of bacteria from mother to infant at birth is assumed to initiate a life-long host-microbe symbiosis. Maternal bacteria are expected to seed the infant intestine and thus play an important role in early development. However, only tracking of strictly defined microbial strains can clarify where the intestinal bacteria come from, how long the initial colonisers persist and whether colonisation by other strains from the environment can replace existing ones. Using rare single nucleotide variants in faecal metagenomes of infants and their family members, we show strong evidence of selective and persistent transmission of maternal strain populations to the vaginally born infant, and their occasional replacement by strains from the environment, including those from family members, in later childhood. Only strains from the classes Actinobacteria and Bacteroidia, which are essential components of the infant microbiome, are transmitted from the mother and persist for at least one year. In contrast, maternal strains of Clostridia, a dominant class in the mother’s gut microbiome, are not observed in the infant. Instead, Clostridia strains are recruited from the environment early on, and fail to colonise persistently until after the first year. Caesarean-born infants showed a striking lack of maternal transmission at birth. For all children analysed, strain influx from the family environment was observed, peaking after the first year. Furthermore, even in adulthood strain sharing between family members, including spouses and siblings, is more common than between unrelated individuals. This suggests that re-colonisation occurs in adulthood. When studying families, fathers appear to be more frequently donors of novel strains to other family members than receivers. Taken together, after selective maternal seeding of the infant gut, species from the environment are recruited, with a rare but continuing strain influx over time.