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A symbiotic physical niche in Drosophila melanogaster regulates stable association of a multi-species gut microbiota

Author

Listed:
  • Ren Dodge

    (Carnegie Institution for Science)

  • Eric W. Jones

    (Simon Fraser University
    University of California)

  • Haolong Zhu

    (Carnegie Institution for Science
    Johns Hopkins University)

  • Benjamin Obadia

    (University of California)

  • Daniel J. Martinez

    (Carnegie Institution for Science)

  • Chenhui Wang

    (Carnegie Institution for Science
    Howard Hughes Medical Institute)

  • Andrés Aranda-Díaz

    (Stanford University)

  • Kevin Aumiller

    (Carnegie Institution for Science
    Johns Hopkins University)

  • Zhexian Liu

    (Johns Hopkins University)

  • Marco Voltolini

    (Lawrence Berkeley National Lab
    Università degli Studi di Milano)

  • Eoin L. Brodie

    (Lawrence Berkeley National Lab)

  • Kerwyn Casey Huang

    (Stanford University
    Stanford University School of Medicine
    Chan Zuckerberg Biohub)

  • Jean M. Carlson

    (University of California)

  • David A. Sivak

    (Simon Fraser University)

  • Allan C. Spradling

    (Carnegie Institution for Science
    Johns Hopkins University
    Howard Hughes Medical Institute)

  • William B. Ludington

    (Carnegie Institution for Science
    Johns Hopkins University)

Abstract

The gut is continuously invaded by diverse bacteria from the diet and the environment, yet microbiome composition is relatively stable over time for host species ranging from mammals to insects, suggesting host-specific factors may selectively maintain key species of bacteria. To investigate host specificity, we used gnotobiotic Drosophila, microbial pulse-chase protocols, and microscopy to investigate the stability of different strains of bacteria in the fly gut. We show that a host-constructed physical niche in the foregut selectively binds bacteria with strain-level specificity, stabilizing their colonization. Primary colonizers saturate the niche and exclude secondary colonizers of the same strain, but initial colonization by Lactobacillus species physically remodels the niche through production of a glycan-rich secretion to favor secondary colonization by unrelated commensals in the Acetobacter genus. Our results provide a mechanistic framework for understanding the establishment and stability of a multi-species intestinal microbiome.

Suggested Citation

  • Ren Dodge & Eric W. Jones & Haolong Zhu & Benjamin Obadia & Daniel J. Martinez & Chenhui Wang & Andrés Aranda-Díaz & Kevin Aumiller & Zhexian Liu & Marco Voltolini & Eoin L. Brodie & Kerwyn Casey Huan, 2023. "A symbiotic physical niche in Drosophila melanogaster regulates stable association of a multi-species gut microbiota," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36942-x
    DOI: 10.1038/s41467-023-36942-x
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    References listed on IDEAS

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