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

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 Huang, Jean M. Carlson, David A. Sivak, Allan C. Spradling and William B. Ludington ()
Additional contact information
Ren Dodge: Carnegie Institution for Science
Eric W. Jones: Simon Fraser University
Haolong Zhu: Carnegie Institution for Science
Benjamin Obadia: University of California
Daniel J. Martinez: Carnegie Institution for Science
Chenhui Wang: Carnegie Institution for Science
Andrés Aranda-Díaz: Stanford University
Kevin Aumiller: Carnegie Institution for Science
Zhexian Liu: Johns Hopkins University
Marco Voltolini: Lawrence Berkeley National Lab
Eoin L. Brodie: Lawrence Berkeley National Lab
Kerwyn Casey Huang: Stanford University
Jean M. Carlson: University of California
David A. Sivak: Simon Fraser University
Allan C. Spradling: Carnegie Institution for Science
William B. Ludington: Carnegie Institution for Science

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-36942-x

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