Residence-colonization trade-off and niche differentiation enable coexistence of Escherichia coli phylogroups in healthy humans

Abstract

Despite abundant literature on pathogenicity and virulence of the opportunistic pathogen Escherichia coli, much less is known about its ecological and evolutionary dynamics as a commensal. Based on two detailed longitudinal datasets on the gut microbiota of healthy adults followed for months to years in France and the USA, we identified a robust trade-off between the ability to establish in a new host (colonization) and to remain in the host (residence). Major E. coli lineages (phylogroups or subgroups) exhibited similar fitness but diverse strategies, from strong colonisers residing few days in the gut to poor colonisers residing for years. Strains with the largest number of extra-intestinal virulence associated genes and highest pathogenicity also resided for longest in hosts. Furthermore, the residence of a strain was more strongly reduced when it competed with other strains from the same phylogroup than from another phylogroup, suggesting niche differentiation between phylogroups. Based on a discrete-state Markov model developed to describe E. coli dynamics in a host population, we found that the trade-off and niche differentiation acted together as equalizing and stabilizing mechanisms allowing phylogroups to coexist over long periods of time. Our model also predicted that external disturbances may disproportionately affect resident strains, such as the extraintestinal pathogenic ones of subgroup B2.3. Our results call for further studies outside high-income countries, where the prevalence of this phylogroup is much lower. More generally, the trade-off between colonization and persistence could play a role in the diversification of other bacterial species of the microbiome.