Evolutionary dynamics of bacteria in a human host environment

TLDR

Laboratory evolution experiments have linked adaptation to genomic change, yet long‑term monitoring in natural systems has been lacking, limiting our understanding of in‑situ evolutionary dynamics. The study aims to characterize the evolutionary dynamics of a Pseudomonas aeruginosa lineage adapting to cystic fibrosis patient airways over 200,000 generations and estimate natural mutation rates. The authors tracked the lineage in multiple patients across 200,000 bacterial generations, providing mutation rate estimates in a natural environment. The lineage exhibited limited diversification, an initial rapid adaptation driven by few pleiotropic mutations, followed by drift and negative selection, suggesting it reached a major adaptive peak and may have transitioned to a primary pathogen in cystic fibrosis patients.

Abstract

Laboratory evolution experiments have led to important findings relating organism adaptation and genomic evolution. However, continuous monitoring of long-term evolution has been lacking for natural systems, limiting our understanding of these processes in situ. Here we characterize the evolutionary dynamics of a lineage of a clinically important opportunistic bacterial pathogen, Pseudomonas aeruginosa, as it adapts to the airways of several individual cystic fibrosis patients over 200,000 bacterial generations, and provide estimates of mutation rates of bacteria in a natural environment. In contrast to predictions based on in vitro evolution experiments, we document limited diversification of the evolving lineage despite a highly structured and complex host environment. Notably, the lineage went through an initial period of rapid adaptation caused by a small number of mutations with pleiotropic effects, followed by a period of genetic drift with limited phenotypic change and a genomic signature of negative selection, suggesting that the evolving lineage has reached a major adaptive peak in the fitness landscape. This contrasts with previous findings of continued positive selection from long-term in vitro evolution experiments. The evolved phenotype of the infecting bacteria further suggests that the opportunistic pathogen has transitioned to become a primary pathogen for cystic fibrosis patients.