Evolutionary dynamics of bacteria in a human host environment

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.

Substantial molecular evolution and mutation rates in prolonged latent Mycobacterium tuberculosis infection in humans

“…Corresponding P-values were calculated under the assumption that the numbers of nonsynonymous and synonymous mutations are independent Poisson random variables (Yang et al, 2011).…”

Insights from genomic comparisons of genetically monomorphic bacterial pathogens

“…aeruginosa during infection of the cystic fibrosis lung may represent source-sink dynamics: the bacteria infecting the sink (the lung) are apparently usually incapable of further transmission to other patients. In those rare cases in which further transmission does occur, continued evolution is neutral after a few initial years of adaptation to a human host [38]. Thus, the lessons taught by experimental evolution may be largely restricted to a short phase of adaptation to a novel environment, and are not applicable to the full dynamics of evolution in existing natural populations.…”

Social complementation and growth advantages promote socially defective bacterial isolates

“…B 281: 20140036 the frequencies and fates of genotypes that differ in social trait expression is challenging. It requires understanding the fitness spectra of such variants across the relevant range of abiotic and biotic environments they encounter (including social environments), as well as the environmental and genetic determinants of those spectra [23,24,29]. Among other factors, social interactions between such variants are likely to significantly affect their fitness dynamics.…”

“…Examples include variation in quorum-sensing signal production in Pseudomonas aeruginosa [18], bioluminescence in Vibrio fisheri [19], and social swarming [20] and spore production [21] in Myxococcus xanthus. However, little is understood regarding how the evolutionary forces of mutation, selection and genetic drift dynamically shape observed forms and levels of such diversity across heterogeneous environments [18,19,[22][23][24][25]. Among other factors, interactions between microbial genotypes that differ in the degree to which they express a social phenotype are likely to influence diversity patterns both within and across groups of interacting individuals.…”