Abstract
Intestinal microbiota perform many functions for their host, but among the most important is their role in metabolism, especially the conversion of recalcitrant biomass that the host is unable to digest into bioavailable compounds. Most studies have focused on the assistance gut microbiota provide in the metabolism of carbohydrates, however, their role in host amino acid metabolism is poorly understood. We conducted an experiment on Mus musculus using 16S rRNA gene sequencing and carbon isotope analysis of essential amino acids (AAESS) to quantify the community composition of gut microbiota and the contribution of carbohydrate carbon used by the gut microbiome to synthesize AAESS that are assimilated by mice to build skeletal muscle tissue. The relative abundances of Firmicutes and Bacteroidetes inversely varied as a function of dietary macromolecular content, with Firmicutes dominating when mice were fed low-protein diets that contained the highest proportions of simple carbohydrates (sucrose). Mixing models estimated that the microbial contribution of AAESS to mouse muscle varied from less than 5% (threonine, lysine, and phenylalanine) to approximately 60% (valine) across diet treatments, with the Firmicute-dominated microbiome associated with the greatest contribution. Our results show that intestinal microbes can provide a significant source of the AAESS their host uses to synthesize structural tissues. The role that gut microbiota play in the amino acid metabolism of animals that consume protein-deficient diets is likely a significant but under-recognized aspect of foraging ecology and physiology.
Highlights
Herbivores and omnivores often consume low-quality diets deficient in the amount and quality of protein that is required to maintain homeostasis and reproduce [1]
Our data show that the degree of AAESS synthesized by the gut microbiome from dietary carbohydrates and used by the host to build structural tissues is strongly correlated with the composition of the microbiome community
Mice used a significant proportion of microbially derived AAESS and had bacterial microbiomes dominated by Firmicutes when fed diets low in protein but full of simple carbohydrates
Summary
Herbivores and omnivores often consume low-quality diets deficient in the amount and quality of protein that is required to maintain homeostasis and reproduce [1]. A similar approach has been applied to phytophagous insects that persistently consume AA-deficient diets [21,22,32] Overall, data from both labelled and natural abundance isotope-based experiments suggest that intestinal bacteria can play a significant role in the protein metabolism of their host. We applied a linear mixing model that incorporated weight per cent diet proportions and associated AAESS concentrations to estimate the availability of dietary AAESS sourced from both casein and cornmeal, which was 10% protein by weight This first model (Model #1) generated treatment-specific δ13C values for AAESS that could be directly routed from diet, which for most diet treatments was overwhelmingly casein but did include a significant cornmeal component in the low-protein diet treatment. A variety of factors such as diet and/or gut microbiome community composition can influence our AA supply calculations, we attempted to use published information for non-ruminant mammals that mimicked our experimental diets in terms of protein type and content
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