TY - JOUR

T1 - Evolutionary dynamics of bacteria in a human host environment

A1 - Yang,Lei

A1 - Jelsbak,Lars

A1 - Marvig,Rasmus Lykke

A1 - Pedersen,Søren Damkiær

A1 - Workman,Christopher

A1 - Rau,Martin Holm

A1 - Hansen,Susse Kirkelund

A1 - Folkesson,Anders

A1 - Johansen,Helle Krogh

A1 - Ciofu,Oana

A1 - Høiby,Niels

A1 - Sommer,Morten

A1 - Molin,Søren

AU - Yang,Lei

AU - Jelsbak,Lars

AU - Marvig,Rasmus Lykke

AU - Pedersen,Søren Damkiær

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

PB - National Academy of Sciences

PY - 2011

Y1 - 2011

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 - Transcriptomics

KW - Genome sequences

KW - Natural population

KW - Chronic infection

KW - Microbial evolution

UR - http://www.pnas.org/

U2 - 10.1073/pnas.1018249108

DO - 10.1073/pnas.1018249108

JO - National Academy of Sciences. Proceedings

JF - National Academy of Sciences. Proceedings

SN - 0027-8424

IS - 18

VL - 108

SP - 7481

EP - 7486

ER -