Evolutionary dynamics of bacteria in a human host environment

Lei Yang; Lars Jelsbak; Rasmus Lykke Marvig; Søren  Damkiær; Christopher Workman; Martin Holm Rau; Susse Kirkelund Hansen; Anders Folkesson; Helle Krogh Johansen; Oana Ciofu; Niels Høiby; Morten Sommer; Søren Molin

doi:10.1073/pnas.1018249108

Evolutionary dynamics of bacteria in a human host environment

Lei Yang, Lars Jelsbak, Rasmus Lykke Marvig, Søren Damkiær, Christopher Workman, Martin Holm Rau, Susse Kirkelund Hansen, Anders Folkesson, Helle Krogh Johansen, Oana Ciofu, Niels Høiby, Morten Sommer, Søren Molin

Department of Immunology and Microbiology

228 Citations (Scopus)

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.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	108
Issue number	18
Pages (from-to)	7481-6
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1018249108 https://doi.org/10.1073/pnas.1018249108
Publication status	Published - 3 May 2011

Keywords

Adaptation, Biological
Base Sequence
Biological Evolution
Cystic Fibrosis
DNA Primers
Gene Expression Profiling
Genetic Drift
Genetic Pleiotropy
Genetic Variation
Genome, Bacterial
Humans
Molecular Sequence Data
Oligonucleotide Array Sequence Analysis
Phenotype
Phylogeny
Polymorphism, Single Nucleotide
Pseudomonas aeruginosa
Selection, Genetic
Sequence Analysis, DNA

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Yang, L., Jelsbak, L., Marvig, R. L., Damkiær, S., Workman, C., Rau, M. H., Hansen, S. K., Folkesson, A., Johansen, H. K., Ciofu, O., Høiby, N., Sommer, M., & Molin, S. (2011). Evolutionary dynamics of bacteria in a human host environment. Proceedings of the National Academy of Sciences of the United States of America, 108(18), 7481-6. https://doi.org/10.1073/pnas.1018249108, https://doi.org/10.1073/pnas.1018249108

Yang, L, Jelsbak, L, Marvig, RL, Damkiær, S, Workman, C, Rau, MH, Hansen, SK, Folkesson, A, Johansen, HK , Ciofu, O , Høiby, N, Sommer, M & Molin, S 2011, 'Evolutionary dynamics of bacteria in a human host environment', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 18, pp. 7481-6. https://doi.org/10.1073/pnas.1018249108, https://doi.org/10.1073/pnas.1018249108

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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.",

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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

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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.

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KW - Base Sequence

KW - Biological Evolution

KW - Cystic Fibrosis

KW - DNA Primers

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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

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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 -

Evolutionary dynamics of bacteria in a human host environment

Abstract

Keywords

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