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Plasmids in the human gut reveal neutral dispersal and recombination that is overpowered by inflammatory diseases

Author

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  • Alvah Zorea

    (Ben-Gurion University of the Negev
    Ben-Gurion University of the Negev
    Ben-Gurion University of the Negev)

  • David Pellow

    (Tel Aviv University)

  • Liron Levin

    (Ben-Gurion University of the Negev)

  • Shai Pilosof

    (Ben-Gurion University of the Negev
    Ben-Gurion University of the Negev)

  • Jonathan Friedman

    (Hebrew University)

  • Ron Shamir

    (Tel Aviv University)

  • Itzhak Mizrahi

    (Ben-Gurion University of the Negev
    Ben-Gurion University of the Negev
    Ben-Gurion University of the Negev)

Abstract

Plasmids are pivotal in driving bacterial evolution through horizontal gene transfer. Here, we investigated 3467 human gut microbiome samples across continents and disease states, analyzing 11,086 plasmids. Our analyses reveal that plasmid dispersal is predominantly stochastic, indicating neutral processes as the primary driver of their wide distribution. We find that only 20-25% of plasmid DNA is being selected in various disease states, constraining its distribution across hosts. Selective pressures shape specific plasmid segments with distinct ecological functions, influenced by plasmid mobilization lifestyle, antibiotic usage, and inflammatory gut diseases. Notably, these elements are more commonly shared within groups of individuals with similar health conditions, such as Inflammatory Bowel Disease (IBD), regardless of geographic location across continents. These segments contain essential genes such as iron transport mechanisms- a distinctive gut signature of IBD that impacts the severity of inflammation. Our findings shed light on mechanisms driving plasmid dispersal and selection in the human gut, highlighting their role as carriers of vital gene pools impacting bacterial hosts and ecosystem dynamics.

Suggested Citation

  • Alvah Zorea & David Pellow & Liron Levin & Shai Pilosof & Jonathan Friedman & Ron Shamir & Itzhak Mizrahi, 2024. "Plasmids in the human gut reveal neutral dispersal and recombination that is overpowered by inflammatory diseases," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47272-x
    DOI: 10.1038/s41467-024-47272-x
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    References listed on IDEAS

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    1. Mislav Acman & Lucy van Dorp & Joanne M. Santini & Francois Balloux, 2020. "Large-scale network analysis captures biological features of bacterial plasmids," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    2. Tanita Wein & Nils F. Hülter & Itzhak Mizrahi & Tal Dagan, 2019. "Emergence of plasmid stability under non-selective conditions maintains antibiotic resistance," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Suzanne Humphrey & Álvaro San Millán & Macarena Toll-Riera & John Connolly & Alejandra Flor-Duro & John Chen & Carles Ubeda & R. Craig MacLean & José R. Penadés, 2021. "Staphylococcal phages and pathogenicity islands drive plasmid evolution," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Emmanuelle Le Chatelier & Trine Nielsen & Junjie Qin & Edi Prifti & Falk Hildebrand & Gwen Falony & Mathieu Almeida & Manimozhiyan Arumugam & Jean-Michel Batto & Sean Kennedy & Pierre Leonard & Junhua, 2013. "Richness of human gut microbiome correlates with metabolic markers," Nature, Nature, vol. 500(7464), pages 541-546, August.
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