Gut Bacteria Mediate Nutrient Availability in Drosophila Diets.

Danielle N A Lesperance,Nichole A Broderick,Andrew J Mcbain

doi:10.1128/aem.01401-20

Danielle N A Lesperance, Nichole A Broderick + Show 1 more

Open Access

https://doi.org/10.1128/aem.01401-20

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Abstract

Drosophila melanogaster gut microbes play important roles in host nutritional physiology. However, these associations are often indirect, and studies typically are in the context of specialized nutritional conditions, making it difficult to discern how microbiome-mediated impacts translate to physiologically relevant conditions, in the laboratory or nature. In this study, we quantified changes in dietary nutrients due to D. melanogaster gut bacteria on three artificial diets and a natural diet of grapes. We show that under all four diet conditions, bacteria altered the protein, carbohydrates, and moisture of the food substrate. An in-depth analysis of one diet revealed that bacteria also increased the levels of tryptophan, an essential amino acid encountered scarcely in nature. These nutrient changes result in an increased protein-to-carbohydrate (P:C) ratio in all diets, which we hypothesized to be a significant determinant of microbiome-mediated host nutritional physiology. To test this, we compared life history traits of axenic flies reared on the three artificial diets with increased P:C ratios or continuous bacterial inoculation. We found that while on some diets, an environment of nutritional plenitude had impacts on life history, it did not fully explain all microbiome-associated phenotypes. This suggests that other factors, such as micronutrients and feeding behavior, likely also contribute to life history traits in a diet-dependent manner. Thus, while some bacterial impacts on nutrition occur across diets, others are dictated by unique dietary environments, highlighting the importance of diet-microbiome interactions in D. melanogaster nutritional physiology.IMPORTANCE Both in the laboratory and in nature, D. melanogaster-associated microbes serve as nutritional effectors, either through the production of metabolites or as direct sources of protein biomass. The relationship between the microbiome and the resulting host nutritional physiology is significantly impacted by diet composition, yet studies involving D. melanogaster are performed using a wide range of artificial diets, making it difficult to discern which aspects of host-microbe interactions may be universal or diet dependent. In this study, we utilized three standard D. melanogaster diets and a natural grape diet to form a comprehensive understanding of the quantifiable nutritional changes mediated by the host microbial community. We then altered these artificial diets based on the observed microbe-mediated changes to demonstrate their potential to influence host physiology, allowing us to identify nutritional factors whose effects were either universal for the three artificial diets or dependent on host diet composition.

Highlights

Gut microbes have important functions in host development, immunity, intestinal homeostasis, and metabolism across model organisms (Belkaid and Harrison, 2017; Gerbaba et al, 2017; Lesperance and Broderick, 2020a; Lin andZhang, 2017)
Treated food was incubated at 25°C for 14 days to simulate the length of time bacteria would associate with food over the course of a typical fly life cycle
Bacterial treatment decreased carbohydrates and increased moisture compared to PBS-treated controls, with generally no significant change in protein, ash, or fat levels (Figure 1A-C, Figure S1A)

Summary

Introduction

Gut microbes have important functions in host development, immunity, intestinal homeostasis, and metabolism across model organisms (Belkaid and Harrison, 2017; Gerbaba et al, 2017; Lesperance and Broderick, 2020a; Lin andZhang, 2017). Use of the Drosophila melanogaster model has revealed significant roles for gut microbes in activating nutritional signaling pathways (Shin et al., 2011; Storelli et al, 2011), stimulating protein nutrition (Keebaugh et al, 2018; Yamada et al, 2015), and catabolizing dietary carbohydrates (Huang and Douglas, 2015). In conditions of nutrient scarcity, gut bacteria decrease development time and increase lifespan (Keebaugh et al, 2018; Shin et al, 2011; Storelli et al, 2011; Yamada et al, 2015). Excess dietary protein is thought to diminish the impact of the microbiome ( bacteria) on development and lifespan (Keebaugh et al, 2019)

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