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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.

SUBMITTER: Gregor R

PROVIDER: S-EPMC9038745 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Mammalian gut metabolomes mirror microbiome composition and host phylogeny.

Gregor Rachel R Probst Maraike M Eyal Stav S Aksenov Alexander A Sasson Goor G Horovitz Igal I Dorrestein Pieter C PC Meijler Michael M MM Mizrahi Itzhak I

The ISME journal 20211213 5

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 conten ...[more]

PMID: 34903850

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Project description:BackgroundInvertebrates are a very attractive subject for studying host-microbe interactions because of their simple gut microbial community and host diversity. Studying the composition of invertebrate gut microbiota and the determining factors is essential for understanding their symbiotic mechanism. Cephalopods are invertebrates that have similar biological properties to vertebrates such as closed circulation system, an advanced nervous system, and a well-differentiated digestive system. However, it is not currently known whether their microbiomes have more in common with vertebrates or invertebrates. This study reports on the microbial composition of six cephalopod species and compares them with other mollusk and marine fish microbiomes to investigate the factors that shape the gut microbiota.ResultsEach cephalopod gut consisted of a distinct consortium of microbes, with Photobacterium and Mycoplasma identified as core taxa. The gut microbial composition of cephalopod reflected their host phylogeny, the importance of which was supported by a detailed oligotype-level analysis of operational taxonomic units assigned to Photobacterium and Mycoplasma. Photobacterium typically inhabited multiple hosts, whereas Mycoplasma tended to show host-specific colonization. Furthermore, we showed that class Cephalopoda has a distinct gut microbial community from those of other mollusk groups or marine fish. We also showed that the gut microbiota of phylum Mollusca was determined by host phylogeny, habitat, and diet.ConclusionWe have provided the first comparative analysis of cephalopod and mollusk gut microbial communities. The gut microbial community of cephalopods is composed of distinctive microbes and is strongly associated with their phylogeny. The Photobacterium and Mycoplasma genera are core taxa within the cephalopod gut microbiota. Collectively, our findings provide evidence that cephalopod and mollusk gut microbiomes reflect host phylogeny, habitat, and diet. It is hoped that these data can contribute to future studies on invertebrate-microbe interactions.

Project description:Background - Prepregnancy overweight and obesity promote deleterious health impacts on both mothers during pregnancy and the offspring. Significant changes in the maternal peripheral blood mononuclear cells (PBMCs) gene expression due to obesity are well-known. However, during pregnancy the impact of overweight on immune cell gene expression and its association with maternal and infant outcomes is not well explored. Methods – Blood samples were collected from healthy normal weight (NW, BMI 18.5-24.9) or overweight (OW, BMI 25-29.9) 2nd parity pregnant women at 12, 24 and 36 weeks of pregnancy. PBMCs were isolated from the blood and subjected to mRNA sequencing. Maternal and infant microbiota were analyzed by 16S rRNA gene sequencing. Integrative multi-omics data analysis was performed to evaluate the association of gene expression with maternal diet, gut microbiota, milk composition, and infant gut microbiota. Results - Gene expression analysis revealed that 453 genes were differentially expressed in the OW women compared to NW women at 12 weeks of pregnancy, out of which 354 were upregulated and 99 were downregulated. Several up-regulated genes in the OW group were enriched in inflammatory, chemokine-mediated signaling and regulation of interleukin-8 production-related pathways. At 36 weeks of pregnancy healthy eating index score was positively associated with several genes that include, DTD1, ELOC, GALNT8, ITGA6-AS1, KRT17P2, NPW, POT1-AS1 and RPL26. In addition, at 36 weeks of pregnancy, genes involved in adipocyte functions, such as NG2 and SMTNL1, were negatively correlated to human milk 2’FL and total fucosylated oligosaccharides content collected at 1 month postnatally. Furthermore, infant Akkermansia was positively associated with maternal PBMC anti-inflammatory genes that include CPS1 and RAB7B, at 12 and 36 weeks of pregnancy. Conclusions – These findings suggest that prepregnancy overweight impacts the immune cell gene expression profile, particularly at 12 weeks of pregnancy. Further, deciphering the complex association of PBMC’s gene expression levels with maternal gut microbiome and milk composition and infant gut microbiome may aid in developing strategies to mitigate obesity-mediated effects.

Dataset Information

Mammalian gut metabolomes mirror microbiome composition and host phylogeny.

Publications

Mammalian gut metabolomes mirror microbiome composition and host phylogeny.

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