Two modes of evolution shape bacterial strain diversity in the mammalian gut for thousands of generations

Here, the authors show that a colonizing bacterial strain evolves in the gut by either generating ecotypes or continuously fixing beneficial mutations. They associate the first mode to metabolic mutations and the second to domestication of bacteriophages that are incorporated into the bacterial genome. How and at what pace bacteria evolve when colonizing healthy hosts remains unclear. Here, by monitoring evolution for more than six thousand generations in the mouse gut, we show that the successful colonization of an invader Escherichia coli depends on the diversity of the existing microbiota and the presence of a closely related strain. Following colonization, two modes of evolution were observed: one in which diversifying selection leads to long-term coexistence of ecotypes and a second in which directional selection propels selective sweeps. These modes can be quantitatively distinguished by the statistics of mutation trajectories. In our experiments, diversifying selection was marked by the emergence of metabolic mutations, and directional selection by acquisition of prophages, which bring their own benefits and costs. In both modes, we observed parallel evolution, with mutation accumulation rates comparable to those typically observed in vitro on similar time scales. Our results show how rapid ecotype formation and phage domestication can be in the mammalian gut.

Automated summary

By monitoring evolution for more than six thousand generations in the mouse gut, the authors show that a colonizing bacterial strain evolves through two modes: one involving metabolic mutations and the other involving the domestication of bacteriophages. The study demonstrates the importance of the microbiota diversity and the presence of related strains in the colonization success of Escherichia coli. The research also highlights the rapid formation of ecotypes and phage domestication in the mammalian gut.