Abstract

BackgroundAnimals are chronically infected by benign and beneficial microorganisms that generally promote animal health through their effects on the nutrition, immune function and other physiological systems of the host. Insight into the host-microbial interactions can be obtained by comparing the traits of animals experimentally deprived of their microbiota and untreated animals. Drosophila melanogaster is an experimentally tractable system to study host-microbial interactions.Methodology/Principal FindingsThe nutritional significance of the microbiota was investigated in D. melanogaster bearing unmanipulated microbiota, demonstrated by 454 sequencing of 16S rRNA amplicons to be dominated by the α-proteobacterium Acetobacter, and experimentally deprived of the microbiota by egg dechorionation (conventional and axenic flies, respectively). In axenic flies, larval development rate was depressed with no effect on adult size relative to conventional flies, indicating that the microbiota promotes larval growth rates. Female fecundity did not differ significantly between conventional and axenic flies, but axenic flies had significantly reduced metabolic rate and altered carbohydrate allocation, including elevated glucose levels.Conclusions/SignificanceWe have shown that elimination of the resident microbiota extends larval development and perturbs energy homeostasis and carbohydrate allocation patterns of of D. melanogaster. Our results indicate that the resident microbiota promotes host nutrition and interacts with the regulation of host metabolism.

Highlights

  • It is increasingly recognized that all animals are chronically infected by microorganisms, and that the resident microbiota, especially the substantial microbial community in the alimentary tract, has major effects on nutrient processing, metabolic signaling and, the health and well-being of the animal host [1,2,3]

  • Conclusions/Significance: We have shown that elimination of the resident microbiota extends larval development and perturbs energy homeostasis and carbohydrate allocation patterns of of D. melanogaster

  • A causal role of the microbiota in animal energy metabolism is indicated by the elevated lipid levels and other indices of metabolic syndrome in wild-type mice infected with the microbiota from individuals that are obese as a consequence of genetic deficiencies in leptin or Tolllike receptor 5 [5,6]

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Summary

Introduction

It is increasingly recognized that all animals are chronically infected by microorganisms, and that the resident microbiota, especially the substantial microbial community in the alimentary tract, has major effects on nutrient processing, metabolic signaling and, the health and well-being of the animal host [1,2,3]. It is experimentally challenging to study the interactions between the resident microbiota and the nutrition of humans and rodent biomedical models because the microbiota of mammals includes hundreds of taxa, many of which are unculturable, with wide variation in composition among individuals [7,8,9]. Simple systems comprising animals bearing one or a few microbial taxa are valuable tools to investigate how resident microorganisms interact with host metabolism [10]. Animals are chronically infected by benign and beneficial microorganisms that generally promote animal health through their effects on the nutrition, immune function and other physiological systems of the host. Drosophila melanogaster is an experimentally tractable system to study host-microbial interactions

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