Mammalian gut metabolomes mirror microbiome composition and host phylogeny

Rachel Gregor,Igal Horovitz,Michael M Meijler,Itzhak Mizrahi,Maraike Probst,Goor Sasson,Stav Eyal,Alexander Aksenov,Pieter C Dorrestein

doi:10.1038/s41396-021-01152-0

Abstract

In the past decade, studies on the mammalian gut microbiome have revealed that different animal species have distinct gut microbial compositions. The functional ramifications of this variation in microbial composition remain unclear: do these taxonomic differences indicate microbial adaptations to host-specific functionality, or are these diverse microbial communities essentially functionally redundant, as has been indicated by previous metagenomics studies? Here, we examine the metabolic content of mammalian gut microbiomes as a direct window into ecosystem function, using an untargeted metabolomics platform to analyze 101 fecal samples from a range of 25 exotic mammalian species in collaboration with a zoological center. We find that mammalian metabolomes are chemically diverse and strongly linked to microbiome composition, and that metabolome composition is further correlated to the phylogeny of the mammalian host. Specific metabolites enriched in different animal species included modified and degraded host and dietary compounds such as bile acids and triterpenoids, as well as fermentation products such as lactate and short-chain fatty acids. Our results suggest that differences in microbial taxonomic composition are indeed translated to host-specific metabolism, indicating that taxonomically distant microbiomes are more functionally diverse than redundant.

Highlights

The variation between human gut microbiomes pales in comparison to the vast diversity of gut microbial communities found across mammalian species [1, 2]
Microbial diversity in mammalian microbiomes has been linked to a variety of traits related to host phylogeny, including host physiology, gut morphology, and in the majority of cases the diet, which is considered a cardinal factor in determining microbiome composition [2,3,4,5,6]
The Mantel correlations between different data principal components analysis (PCA) using Euclidean distances was performed on the peak feature abundance tables for the LC–MS/MS and gas chromatography–mass spectrometry (GC–MS) data (Supplementary Fig. S5), and the top and bottom percentiles of loadings for PC1 and PC2 were extracted in order to determine the metabolite features which contributed most to the separation along these axes (Supplementary Fig. S6)

Summary

INTRODUCTION

The variation between human gut microbiomes pales in comparison to the vast diversity of gut microbial communities found across mammalian species [1, 2]. The most comprehensive metagenomics study of mammalian gut microbiomes to date found a large shared core of functional annotations across host species, indicating that despite drastic differences in microbial composition, these communities have similar metabolic potential [14]. Functional redundancy at the metagenome level has been found in a range of microbial environments, including hostassociated environments such as the human gut microbiome [15, 16] and the rumen [17], as well as in environmental samples from the ocean [18] and soil [19] These findings call into question basic assumptions about the relevance of taxonomic differences to ecosystem function [20, 21]. Occasional fruits and vegetables taxonomic diversity and metabolic output in mammalian gut microbiomes by analyzing 101 fecal samples from a range of mammalian species, using an untargeted metabolomics platform together with 16S rRNA gene amplicon sequencing. Our results indicate that differences in microbial taxonomic composition are translated to host-specific microbial metabolism, suggesting that taxonomically distant microbiomes are not functionally redundant

MATERIALS AND METHODS

RESULTS

Findings

DISCUSSION