Evolutionary dynamics of bacteria in a human host environment

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

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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.
    Original languageEnglish
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume108
    Issue number18
    Pages (from-to)7481-7486
    ISSN0027-8424
    DOIs
    Publication statusPublished - 2011

    Keywords

    • Transcriptomics
    • Genome sequences
    • Natural population
    • Chronic infection
    • Microbial evolution

    Cite this

    Yang, Lei ; Jelsbak, Lars ; Marvig, Rasmus Lykke ; Pedersen, Søren Damkiær ; Workman, Christopher ; Rau, Martin Holm ; Hansen, Susse Kirkelund ; Folkesson, Anders ; Johansen, Helle Krogh ; Ciofu, Oana ; Høiby, Niels ; Sommer, Morten ; Molin, Søren. / Evolutionary dynamics of bacteria in a human host environment. In: Proceedings of the National Academy of Sciences of the United States of America. 2011 ; Vol. 108, No. 18. pp. 7481-7486.
    @article{50db68b90f1e4227a2ef9ad6ed502023,
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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.",
    keywords = "Transcriptomics, Genome sequences, Natural population, Chronic infection, Microbial evolution",
    author = "Lei Yang and Lars Jelsbak and Marvig, {Rasmus Lykke} and Pedersen, {S{\o}ren Damki{\ae}r} and Christopher Workman and Rau, {Martin Holm} and Hansen, {Susse Kirkelund} and Anders Folkesson and Johansen, {Helle Krogh} and Oana Ciofu and Niels H{\o}iby and Morten Sommer and S{\o}ren Molin",
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    Evolutionary dynamics of bacteria in a human host environment. / Yang, Lei; Jelsbak, Lars; Marvig, Rasmus Lykke; Pedersen, Søren Damkiær; Workman, Christopher; Rau, Martin Holm; Hansen, Susse Kirkelund; Folkesson, Anders; Johansen, Helle Krogh; Ciofu, Oana; Høiby, Niels; Sommer, Morten; Molin, Søren.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 18, 2011, p. 7481-7486.

    Research output: Contribution to journalJournal articleResearchpeer-review

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    T1 - Evolutionary dynamics of bacteria in a human host environment

    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

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    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

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    DO - 10.1073/pnas.1018249108

    M3 - Journal article

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    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

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