Abstract
Most metazoans engage in mutualistic interactions with their intestinal microbiota. Despite recent progress the molecular mechanisms through which microbiota exerts its beneficial influences on host physiology are still largely uncharacterized. Here we use axenic Drosophila melanogaster adults associated with a standardized microbiota composed of a defined set of commensal bacterial strains to study the impact of microbiota association on its host transcriptome. Our results demonstrate that Drosophila microbiota has a marked impact on the midgut transcriptome and promotes the expression of genes involved in host digestive functions and primary metabolism. We identify the IMD/Relish signaling pathway as a central regulator of this microbiota-mediated transcriptional response and we reveal a marked transcriptional trade-off between the midgut response to its beneficial microbiota and to bacterial pathogens. Taken together our results indicate that microbiota association potentiates host nutrition and host metabolic state, two key physiological parameters influencing host fitness. Our work paves the way to subsequent mechanistic studies to reveal how these microbiota-dependent transcriptional signatures translate into host physiological benefits.
Highlights
Metazoans establish functional interactions with their microbiota, the dynamic microbial communities that colonize their mucosal surfaces
Since the microbiota load and composition encountered in conventionally laboratory-reared flies (CONV) fluctuate highly [9,17], we chose to associate newly emerged GF adults with a standardized microbiota composed of four previously characterized Drosophila commensal bacterial strains (Acetobacter pomorum, Commensalibacter intestini, Lactobacillus brevis and Lactobacillus plantarum) [18] (Fig.1A)
After data normalization and statistical analysis using Significance Analysis of Microarrays (SAM), using a false detection rate (FDR) of 0,2, we identified 105 transcripts whose expression level were significantly increased from 1.2 to 6 folds in the polyassociated flies compared to their GF siblings (Fig.1B and Fig.2)
Summary
Metazoans establish functional interactions with their microbiota, the dynamic microbial communities that colonize their mucosal surfaces. These interactions contribute to many aspects of host physiology, notably metabolism and immunity [1]. The molecular mechanisms through which the microbiota exerts its beneficial influences on host physiology are still largely undefined. Drosophila melanogaster has emerged as a powerful model to study host-microbiota interactions [2,3]. The ease to manipulate Drosophila commensal bacterial species and to cultivate Germ-Free (GF) animals, coupled to its powerful genetic tools makes Drosophila an ideal host model to study molecular mechanisms underlying microbiota-mediated physiological benefits
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