Analysis of human fecal metagenomes from adults and infants, to investigate strain persistance, dispersal and purifying selection of bacterial strains.

Some gut bacteria remain associated with their human host for years while others are rapidly displaced. To understand strain persistence and dispersal, we analysed gut bacteria from longitudinally-collected adult and infant faecal samples; from 5,278 metagenomes we constructed 130,862 strain-resolved metagenomic species (sMGS), representing the 440 most prevalent gut commensals. Universally there was high strain persistence (mean annual survival rate: 95%). Bacterial persistence was greater in adults than infants, and strongly correlated to the colonisation of proximal hosts. Occasionally persistence was associated to even wider geographic neighbourhoods, typically at a regional scale (< 150 km radius). While vertical (parent-child) and horizontal (parent-parent) strain sharing was common among all phyla, highly persistent taxa were preferentially vertically shared. Bifidobacterium, Methanobrevibacter and Sutterella had the strongest family associations. Sporulation capacity and oxidative tolerance were negatively correlated with persistence, although the ability to sporulate increased family colonisation rate. Strain persistence correlated with fewer genetic bottlenecks and higher rates of purifying selection, indicating a decreased mutational burden.This data suggests that Firmicutes, often sporulation competent, have the most dynamic strain exchange and loss pattern, with less geographic restrictions, while Bacteroidota, like Prevotella and Bacteroides, have a key role in the gut colonization, as they are characterized by restricted dispersal, high family sharing and vertical transmission, and a higher resilience to strain exchanges during life and especially in the infant microbiome. We define here such species as “tenacious” commensals, which possess all the hallmarks of highly adapted species.