Microbes Promote Amino Acid Harvest to Rescue Undernutrition in Drosophila

Abstract

Summary Microbes play an important role in the pathogenesis of nutritional disorders such as protein-specific malnutrition. However, the precise contribution of microbes to host energy balance during undernutrition is unclear. Here, we show that Issatchenkia orientalis, a fungal microbe isolated from field-caught Drosophila melanogaster, promotes amino acid harvest to rescue the lifespan of undernourished flies. Using radioisotope-labeled dietary components (amino acids, nucleotides, and sucrose) to quantify nutrient transfer from food to microbe to fly, we demonstrate that I. orientalis extracts amino acids directly from nutrient-poor diets and increases protein flux to the fly. This microbial association restores body mass, protein, glycerol, and ATP levels and phenocopies the metabolic profile of adequately fed flies. Our study uncovers amino acid harvest as a fundamental mechanism linking microbial and host metabolism, and highlights Drosophila as a platform for quantitative studies of host-microbe relationships.

Distinct Shifts in Microbiota Composition during Drosophila Aging Impair Intestinal Function and Drive Mortality

“…However, these issues highlight the complexity of the host-microbe interaction and its impact on host lifespan. Beneficial contributions of microbes to fly health seem to be highly dependent on nutrient conditions—we recently demonstrated that gut-associated microbes promote amino acid harvest to rescue lifespan during undernutrition (Yamada et al, 2015). Hence, it is possible that the presence of gut-associated microbes can be beneficial or deleterious to host lifespan depending on the nutrient environment.…”

Preventing Age-Related Decline of Gut Compartmentalization Limits Microbiota Dysbiosis and Extends Lifespan

“…The lifespan extension observed when JAK/STAT was reduced in the CCR of sterile flies indicates broader beneficial consequences of this perturbation that may result from improved food digestion and nutrient assimilation. Furthermore, since microbes also have a beneficial effect on fly nutrition (Yamada et al, 2015), it is likely that the metabolic consequences of age-related gastric decline are complex and provide interesting grounds for future studies.…”

Stable Host Gene Expression in the Gut of Adult Drosophila melanogaster with Different Bacterial Mono-Associations

“…Additionally, flies appear to lack the crypt structures, present in vertebrate guts, that can provide hideout for microbes allowing them to persist during hard times [35]. At present, we know that lab-reared flies can lose their microbiota by continually transferring onto sterile food [28,38]. The turnover of fly microbiota under these conditions suggests that stable colonization of the gut tissue is not occurring under these circumstances, although it is possible that there are different conditions under which stable colonization could be observed.…”

“…Yamada et al (2015) discovered that a yeast species, Issatchenki orientalis , increases amino acid availability and extends lifespan in flies reared on a protein-deficient diet [38]. They found that lifespan could be extended not just by providing flies with live I .…”