TY - JOUR

T1 - Adaptive Evolution of Pseudomonas aeruginosa in Human Airways Shows Phenotypic Convergence Despite Diverse Patterns of Genomic Changes

AU - Espaillat, Akbar

AU - Colque, Claudia Antonella

AU - Rago, Daniela

AU - La Rosa, Ruggero

AU - Molin, Søren

AU - Johansen, Helle Krogh

N1 - © The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

PY - 2024

Y1 - 2024

N2 - Selective forces in the environment drive bacterial adaptation to novel niches, choosing the fitter variants in the population. However, in dynamic and changing environments, the evolutionary processes controlling bacterial adaptation are difficult to monitor. Here, we follow 9 people with cystic fibrosis chronically infected with Pseudomonas aeruginosa, as a proxy for bacterial adaptation. We identify and describe the bacterial changes and evolution occurring between 15 and 35 yr of within-host evolution. We combine whole-genome sequencing, RNA sequencing, and metabolomics and compare the evolutionary trajectories directed by the adaptation of 4 different P. aeruginosa lineages to the lung. Our data suggest divergent evolution at the genomic level for most of the genes, with signs of convergent evolution with respect to the acquisition of mutations in regulatory genes, which drive the transcriptional and metabolomic program at late time of evolution. Metabolomics further confirmed convergent adaptive phenotypic evolution as documented by the reduction of the quorum-sensing molecules acyl-homoserine lactone, phenazines, and rhamnolipids (except for quinolones). The modulation of the quorum-sensing repertoire suggests that similar selective forces characterize at late times of evolution independent of the patient. Collectively, our data suggest that similar environments and similar P. aeruginosa populations in the patients at prolonged time of infection are associated with an overall reduction of virulence-associated features and phenotypic convergence.

AB - Selective forces in the environment drive bacterial adaptation to novel niches, choosing the fitter variants in the population. However, in dynamic and changing environments, the evolutionary processes controlling bacterial adaptation are difficult to monitor. Here, we follow 9 people with cystic fibrosis chronically infected with Pseudomonas aeruginosa, as a proxy for bacterial adaptation. We identify and describe the bacterial changes and evolution occurring between 15 and 35 yr of within-host evolution. We combine whole-genome sequencing, RNA sequencing, and metabolomics and compare the evolutionary trajectories directed by the adaptation of 4 different P. aeruginosa lineages to the lung. Our data suggest divergent evolution at the genomic level for most of the genes, with signs of convergent evolution with respect to the acquisition of mutations in regulatory genes, which drive the transcriptional and metabolomic program at late time of evolution. Metabolomics further confirmed convergent adaptive phenotypic evolution as documented by the reduction of the quorum-sensing molecules acyl-homoserine lactone, phenazines, and rhamnolipids (except for quinolones). The modulation of the quorum-sensing repertoire suggests that similar selective forces characterize at late times of evolution independent of the patient. Collectively, our data suggest that similar environments and similar P. aeruginosa populations in the patients at prolonged time of infection are associated with an overall reduction of virulence-associated features and phenotypic convergence.

KW - Humans

KW - Pseudomonas aeruginosa/genetics

KW - Cystic Fibrosis/complications

KW - Lung/microbiology

KW - Genomics

KW - Mutation

U2 - 10.1093/molbev/msae022

DO - 10.1093/molbev/msae022

M3 - Journal article

C2 - 38366124

VL - 41

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 2

ER -