Drosophila-associated bacteria differentially shape the nutritional requirements of their host during juvenile growth

PLoS Biol. 2020 Mar 20;18(3):e3000681. doi: 10.1371/journal.pbio.3000681. eCollection 2020 Mar.

Abstract

The interplay between nutrition and the microbial communities colonizing the gastrointestinal tract (i.e., gut microbiota) determines juvenile growth trajectory. Nutritional deficiencies trigger developmental delays, and an immature gut microbiota is a hallmark of pathologies related to childhood undernutrition. However, how host-associated bacteria modulate the impact of nutrition on juvenile growth remains elusive. Here, using gnotobiotic Drosophila melanogaster larvae independently associated with Acetobacter pomorumWJL (ApWJL) and Lactobacillus plantarumNC8 (LpNC8), 2 model Drosophila-associated bacteria, we performed a large-scale, systematic nutritional screen based on larval growth in 40 different and precisely controlled nutritional environments. We combined these results with genome-based metabolic network reconstruction to define the biosynthetic capacities of Drosophila germ-free (GF) larvae and its 2 bacterial partners. We first established that ApWJL and LpNC8 differentially fulfill the nutritional requirements of the ex-GF larvae and parsed such difference down to individual amino acids, vitamins, other micronutrients, and trace metals. We found that Drosophila-associated bacteria not only fortify the host's diet with essential nutrients but, in specific instances, functionally compensate for host auxotrophies by either providing a metabolic intermediate or nutrient derivative to the host or by uptaking, concentrating, and delivering contaminant traces of micronutrients. Our systematic work reveals that beyond the molecular dialogue engaged between the host and its bacterial partners, Drosophila and its associated bacteria establish an integrated nutritional network relying on nutrient provision and utilization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetobacter / genetics
  • Acetobacter / metabolism
  • Acetobacter / physiology*
  • Amino Acids / metabolism
  • Animal Nutritional Physiological Phenomena
  • Animals
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Drosophila melanogaster / microbiology*
  • Drosophila melanogaster / physiology*
  • Gastrointestinal Microbiome
  • Host Microbial Interactions
  • Lactobacillus / genetics
  • Lactobacillus / metabolism
  • Lactobacillus / physiology*
  • Larva / growth & development
  • Larva / metabolism
  • Larva / microbiology
  • Larva / physiology
  • Metabolic Networks and Pathways
  • Micronutrients / metabolism
  • Nutritional Requirements / physiology*
  • Species Specificity

Substances

  • Amino Acids
  • Micronutrients

Grants and funding

Research in FL’s lab is supported by the “Fondation pour la Recherche Médicale” (Equipe FRM DEQ20180339196) and the Scientific Breakthrough Project from Université de Lyon "Microbehave." Research in PdS and FC’s labs are supported by INRA and INSA Lyon. JC is funded by a postdoctoral fellowship from the "Fondation pour la Recherche Médicale" (FRM, SPF20170938612). TG is funded by a PhD fellowship from ENS de Lyon. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.