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.

Highlights

  • Nutrition is the major environmental factor that determines to what extent an organism can realize its genetically-encoded growth potential [1]

  • We have unraveled the interactions between the nutritional environment of D. melanogaster and 2 of its associated bacteria, as well as the functional importance of these interactions for Drosophila juvenile growth

  • We show that both bacteria, each in its unique manner, alleviate the nutritional constraints in the environment to Drosophila-associated bacteria differentially shape their host’s nutritional requirements accelerate host growth and maturation in diets depleted in essential nutrients (Fig 7)

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Summary

Introduction

Nutrition is the major environmental factor that determines to what extent an organism can realize its genetically-encoded growth potential [1]. Drosophila-associated bacteria differentially shape their host’s nutritional requirements

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