Mammalian gut metabolomes mirror microbiome composition and host phylogeny

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.

Annotation-free discovery of functional groups in microbial communities

“…One of the most compelling potential applications of EQO is the identification of functional groups responsible for the production or consumption of metabolites in gut microbiome data. We leveraged an animal gut microbiome dataset with 101 fecal samples from a wide range of 25 mammalian species, accompanied by 74 peak features that are detected by GC-MS in >80% samples 20 . Unlike the case of nitrate discussed above, which has been a major focus of research in since the early days of environmental microbiology, the metabolic processes that drive the production or consumption of metabolites in animal guts are much less understood.…”

“…If the environment is constant across samples, the approach we present in this paper can identify groups of taxa that are most stably maintained across replicates, likely representing ‘species portfolios’ with redundant function. Below we provide a detailed explanation of the approach and show how it can successfully be applied across various data sets, ranging from replicate microcosms 4 to the TARA Oceans microbiome 19 to metabolomic profiles of animal gut microbiomes 20 .…”

High-Altitude Drives the Convergent Evolution of Alpha Diversity and Indicator Microbiota in the Gut Microbiomes of Ungulates

“…The gut microbiome can provide energy, in the form of short-chain fatty acids, to its host and maintain the gut homeostatic balance ( Gonçalves et al, 2018 ; Markowiak-Kopeć and Śliżewska, 2020 ). Many factors affect gut microbiome composition and function, including diet ( Huang et al, 2022 ), phylogeny ( Wang et al, 2019 ; Gregor et al, 2022 ), and environment ( Gacesa et al, 2022 ; Wang et al, 2022 ). When a factor surpasses the other influencing factors, the gut microbiome converges to adapt toward this dominant factor.…”

“…In addition to animals with specialized diets, species with closer phylogenetic relationships or similar behavior have similar gut microbiome compositions ( Gregor et al, 2022 ). Amato et al (2019) found that host phylogeny outweighs the dietary niche in structuring primate gut microbiomes.…”

The Application of Quantitative Metabolomics for the Taxonomic Differentiation of Birds

“…Several recent papers have proposed to use the metabolomic approach for the classification of species. This approach has primarily been applied to plant species and subspecies [ 9 , 10 , 11 , 12 , 13 , 14 , 15 ] (the approach has been known in phytochemistry since the 1960s as ‘chemotaxonomy’) and to a lesser extent to fungi species [ 16 , 17 ], animal microbiomes [ 18 ] and human microbiomes [ 19 ]. Among these papers, some authors used an integrative approach—a combination of metabolomics with genome sequence analyses [ 10 , 11 , 12 , 16 , 18 , 19 ].…”