Residence-colonization trade-off and niche differentiation enable the coexistence ofEscherichia coliphylogroups in healthy humans

Abstract

Despite the extensive literature on the pathogenicity and virulence of the commensal bacterial species and major pathogen Escherichia coli, much less is known about its natural ecological and evolutionary dynamics in populations of healthy hosts. Based on remarkably detailed longitudinal data on the gut microbiota of eight healthy individuals over months to years, we identified a trade-off between colonization and persistence, with major E. coli strains (phylogroups) exhibiting a diversity of strategy from strong colonizers persisting for a few days, to poor colonizers persisting for years in the gut. All phylogroups exhibited similar fitness along the trade-off. Moreover, the persistence time was reduced more strongly when a focal strain competed with other strains of the same phylogroups than of different phylogroups, suggesting niche differentiation within the host. To derive the dynamical consequences of the trade-off and niche differentiation for coexistence between strains, we developed a discrete-state Markov model describing the dynamics of E. coli in a population of hosts. The trade-off and niche differentiation act together as equalizing and stabilizing mechanisms enabling the stable coexistence of phylogroups over extended periods of time. Strains with the largest number of virulence genes and highest pathogenicity are those persisting for longer in hosts. Our model predicts that a reduction in transmission (e.g., through better hygiene) would not alter the balance between phylogroups, while less disturbance of the microbiome favors persisters, such as those belonging to the pathogenic phylogroup B2.3. More generally, the trade-off between colonization and persistence could play a role in the diversification of other bacterial species of the microbiome.

Strain intrinsic properties and environmental constraints together shape Escherichia coli dynamics and diversity over a twenty-year human gut time series

“…A re-analysis of the data from Martinson and Walk [49] showed that the long persistence of some phylogroups was counterbalanced by a poorer capacity to colonize hosts. This persistence-colonization trade-off, together with an additional mechanism of niche differentiation, could in theory explain the coexistence of multiple E. coli phylogroups in the population [75].…”