Isotopic and genetic methods reveal the role of the gut microbiome in mammalian host essential amino acid metabolism

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 (AA ESS ) to quantify the community composition of gut microbiota and the contribution of carbohydrate carbon used by the gut microbiome to synthesize AA ESS 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 AA ESS 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 AA ESS 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.

Dietary protein content and digestibility influences discrimination of amino acid nitrogen isotope values in a terrestrial omnivorous mammal

“…This scenario is unlikely, however, because (1) the need for de novo synthesis should decline as the availability of dietary AA increases, and (2) Δ 15 N Consumer‐Diet values were large for essential AA (Ile, Val, Phe) which cannot be synthesized de novo by mice. The AA δ 15 N values could have also been influenced by the contribution of microbially‐synthesized AA, 26–28 although the reliance on this alternative AA source is also expected to decline as dietary protein increases.…”

Gut microbiota of frugo-folivorous sifakas across environments

“…Across species, the capacity for microbially synthesized amino acids varies by host feeding strategy [ 2 ]. Moreover, reducing dietary protein, while boosting dietary carbohydrates, can lead to greater de novo biosynthesis by gut microbiota of essential amino acids, especially valine [ 70 ]. That captive sifakas in our study had significantly reduced capacity for valine biosynthesis, compared to their wild peers, might suggest that provisioned diets are richer in protein (including e.g., nuts, beans, and chow).…”

Intraspecific variation and energy channel coupling within a Chilean kelp forest

“…Although we found good separation here between Ulva and phytoplankton/POM, our previous work in Alaska (Elliott Smith et al 2018) has noted difficulties in distinguishing among these primary producer groups in EAA δ 13 C multivariate space, and the importance of Ulva to subtidal fish taxa should thus be verified with additional studies. Finally, it should be noted that we cannot account for the potential synthesis of EAA by microbial communities, either within the gut (e.g., Newsome et al 2011, 2020), or during the decomposition of particulate organic matter. Although we currently know very little about the contribution of these microbial communities to the EAA budget of wild consumers, it is possible that this accounts for some of our signal here.…”

“…The analysis of individual essential amino acids (EAA) is particularly useful for community ecology, as these molecules are a major conduit of energy flow between trophic levels (Larsen et al 2009, Ruess and Müller‐Navarra 2019). Because only autotrophs and microbes can synthesize EAA, higher order consumers must acquire them via direct consumption (Fantle et al 1999, Howland et al 2003) or possibly from their gut microbiome if dietary protein content is insufficient (Newsome et al 2011, 2020). Consequently, EAA are minimally altered by consumers during assimilation and the isotopic composition of these molecules remains consistent across trophic linkages (Fantle et al 1999, Howland et al 2003).…”