TY - JOUR
T1 - Evolutionary dynamics of bacteria in a human host environment
AU - Yang, Lei
AU - Jelsbak, Lars
AU - Marvig, Rasmus Lykke
AU - Damkiær, Søren
AU - Workman, Christopher
AU - Rau, Martin Holm
AU - Hansen, Susse Kirkelund
AU - Folkesson, Anders
AU - Johansen, Helle Krogh
AU - Ciofu, Oana
AU - Høiby, Niels
AU - Sommer, Morten
AU - Molin, Søren
PY - 2011/5/3
Y1 - 2011/5/3
N2 - 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.
AB - 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.
KW - Adaptation, Biological
KW - Base Sequence
KW - Biological Evolution
KW - Cystic Fibrosis
KW - DNA Primers
KW - Gene Expression Profiling
KW - Genetic Drift
KW - Genetic Pleiotropy
KW - Genetic Variation
KW - Genome, Bacterial
KW - Humans
KW - Molecular Sequence Data
KW - Oligonucleotide Array Sequence Analysis
KW - Phenotype
KW - Phylogeny
KW - Polymorphism, Single Nucleotide
KW - Pseudomonas aeruginosa
KW - Selection, Genetic
KW - Sequence Analysis, DNA
U2 - 10.1073/pnas.1018249108
DO - 10.1073/pnas.1018249108
M3 - Journal article
C2 - 21518885
SN - 0027-8424
VL - 108
SP - 7481
EP - 7486
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 18
ER -