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The defensome of complex bacterial communities

Author

Listed:
  • Angelina Beavogui

    (Université Paris-Saclay)

  • Auriane Lacroix

    (Université Paris-Saclay)

  • Nicolas Wiart

    (Université Paris-Saclay)

  • Julie Poulain

    (Université Paris-Saclay
    FR2022 / Tara GOsee)

  • Tom O. Delmont

    (Université Paris-Saclay
    FR2022 / Tara GOsee)

  • Lucas Paoli

    (Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich
    Molecular Diversity of Microbes lab)

  • Patrick Wincker

    (Université Paris-Saclay
    FR2022 / Tara GOsee)

  • Pedro H. Oliveira

    (Université Paris-Saclay)

Abstract

Bacteria have developed various defense mechanisms to avoid infection and killing in response to the fast evolution and turnover of viruses and other genetic parasites. Such pan-immune system (defensome) encompasses a growing number of defense lines that include well-studied innate and adaptive systems such as restriction-modification, CRISPR-Cas and abortive infection, but also newly found ones whose mechanisms are still poorly understood. While the abundance and distribution of defense systems is well-known in complete and culturable genomes, there is a void in our understanding of their diversity and richness in complex microbial communities. Here we performed a large-scale in-depth analysis of the defensomes of 7759 high-quality bacterial population genomes reconstructed from soil, marine, and human gut environments. We observed a wide variation in the frequency and nature of the defensome among large phyla, which correlated with lifestyle, genome size, habitat, and geographic background. The defensome’s genetic mobility, its clustering in defense islands, and genetic variability was found to be system-specific and shaped by the bacterial environment. Hence, our results provide a detailed picture of the multiple immune barriers present in environmentally distinct bacterial communities and set the stage for subsequent identification of novel and ingenious strategies of diversification among uncultivated microbes.

Suggested Citation

  • Angelina Beavogui & Auriane Lacroix & Nicolas Wiart & Julie Poulain & Tom O. Delmont & Lucas Paoli & Patrick Wincker & Pedro H. Oliveira, 2024. "The defensome of complex bacterial communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46489-0
    DOI: 10.1038/s41467-024-46489-0
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    1. Santiago Redondo-Salvo & Raúl Fernández-López & Raúl Ruiz & Luis Vielva & María de Toro & Eduardo P. C. Rocha & M. Pilar Garcillán-Barcia & Fernando de la Cruz, 2020. "Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Gene W. Tyson & Jarrod Chapman & Philip Hugenholtz & Eric E. Allen & Rachna J. Ram & Paul M. Richardson & Victor V. Solovyev & Edward M. Rubin & Daniel S. Rokhsar & Jillian F. Banfield, 2004. "Community structure and metabolism through reconstruction of microbial genomes from the environment," Nature, Nature, vol. 428(6978), pages 37-43, March.
    3. Florian Tesson & Alexandre Hervé & Ernest Mordret & Marie Touchon & Camille d’Humières & Jean Cury & Aude Bernheim, 2022. "Systematic and quantitative view of the antiviral arsenal of prokaryotes," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    4. Sean R Eddy, 2008. "A Probabilistic Model of Local Sequence Alignment That Simplifies Statistical Significance Estimation," PLOS Computational Biology, Public Library of Science, vol. 4(5), pages 1-14, May.
    5. Lucas Paoli & Hans-Joachim Ruscheweyh & Clarissa C. Forneris & Florian Hubrich & Satria Kautsar & Agneya Bhushan & Alessandro Lotti & Quentin Clayssen & Guillem Salazar & Alessio Milanese & Charlotte , 2022. "Biosynthetic potential of the global ocean microbiome," Nature, Nature, vol. 607(7917), pages 111-118, July.
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