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

• Published in: Nature communications 2023-03, Vol.14 (1), p.1557-1557, Article 1557
• Main Authors: Dodge, Ren, Jones, Eric W., Zhu, Haolong, Obadia, Benjamin, Martinez, Daniel J., Wang, Chenhui, Aranda-Díaz, Andrés, Aumiller, Kevin, Liu, Zhexian, Voltolini, Marco, Brodie, Eoin L., Huang, Kerwyn Casey, Carlson, Jean M., Sivak, David A., Spradling, Allan C., Ludington, William B.
• Format: Article
• Language: English
• Subjects: 14; 14/19; 14/28; 14/35; 14/63; 14/69; 631/136; 631/326/2565/547; Animals; Bacteria; BASIC BIOLOGICAL SCIENCES; Colonization; Commensals; developmental biology; Diet; Digestive system; Drosophila; Drosophila melanogaster - microbiology; Esophagus; Foregut; Fruit flies; Gastrointestinal Microbiome; Gastrointestinal tract; Gastrointestinal Tract - microbiology; Glycan; Gnotobiotic; Host specificity; Humanities and Social Sciences; Insects; Intestinal microflora; Mammals; Microbiomes; Microbiota; Microorganisms; multidisciplinary; Niches; Science; Science (multidisciplinary); Species; Stability; symbiosis
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-36942-x

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. Animal gut microbiomes are fairly stable over time despite large daily fluctuations in diet and introductions of environmental bacteria. Here the authors report that fruit flies maintain the stability of their microbiome in part through a physical niche in the esophagus.