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Primate gut microbiota induce evolutionarily salient changes in mouse neurodevelopment

ABSTRACT: Multiple primate species, including humans, evolved brains that are exceptionally large relative to their body sizes. These large brains coevolved with metabolic adaptations that enhance cerebral energy supply, including increased circulating glucose levels. While the gut microbiota (GM) is known to influence host metabolism, its potential role in primate brain evolution remains unclear. To investigate this, we inoculated germ-free mice with the GMs of primate species selected to separate the effects of brain size (encephalization) from phylogenetic relatedness: humans (large-brained, Catarrhini), macaques (smaller-brained, Catarrhini), and squirrel monkeys (large-brained, Platyrrhini). We first show that differences in brain gene expression between mice inoculated with human versus macaque GMs resemble those observed between actual human and macaque brains. Comparing the effects of the different primate GMs on mouse brain gene expression further revealed that, despite greater evolutionary distance, the GMs from the two larger-brained species (humans and squirrel monkeys) similarly upregulated genes associated with energy production. Notably, human GMs specifically increased the expression of genes involved in oxidative phosphorylation, and these gene expression changes correlated with increased abundances of GM metabolic pathways related to glucose metabolism and gluconeogenesis. Human GMs also downregulated evolutionarily conserved genes implicated in neurodevelopmental disorders such as autism. Although these are findings based on a small sample of primate species and must be interpreted as preliminary, they suggest that species differences in GM composition can influence brain metabolism and raise the possibility that the GM could have played a supporting role in primate encephalization.

ORGANISM(S): Mus musculus

PROVIDER: GSE312570 | GEO | 2025/12/08

REPOSITORIES: GEO

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Project description:Objective: The dietary xanthophylls, lutein and zeaxanthin, accumulate in primate brain and may be beneficial for cognition. Brain xanthophyll content varies greatly among individuals and genetic factors are likely to be significant contributors. Subspecies of rhesus macaques originating from different geographic locations differ genetically, but the effect of origin on gene expression and carotenoid status has not been determined. The study objective was to determine whether xanthophyll status and expression of carotenoid-related genes, as well as genes with known variants between subspecies, differ between the brains of adult rhesus monkeys of Indian and Chinese origin. Methods: Next generation RNA sequencing was used to determine differentially expressed carotenoid-related genes and genes with known variants among rhesus monkey subspecies in the prefrontal cortex, cerebellum, and striatum of Indian-origin monkeys (n=3) versus Chinese-origin monkeys (n=3). Serum and brain xanthophylls were determined using HPLC. FastQC was performed on raw sequenced reads to determine the quality of each read. Reads were mapped to the Rhesus Macaque reference genome and differences in gene expression (FPKM) were determined using TopHat and Cuffdiff, respectively. Findings from RNAseq were validated using RT-PCR. Results: Indian-origin monkeys had higher xanthophyll levels in brain tissue compared to Chinese-origin monkeys despite consuming similar amounts of dietary carotenoids. In a region-specific manner, 4 genes related to carotenoid and fatty acid metabolism (BCO2, RPE65, ELOVL4, FADS2) and 4 genes involved in the immune response (CD4, CD74, CXCL12 LTBR) were differentially expressed between Indian- and Chinese-origin monkeys. Expression of all four genes involved in carotenoid and fatty acid metabolism were correlated with brain xanthophyll concentration in a region-specific manner. Conclusions: These results indicate that origin is related to differences in both gene expression and xanthophyll content in the brain. Findings from this study may have important implications regarding genetic diversity, lutein status, and cognition in primates.

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Primate gut microbiota induce evolutionarily salient changes in mouse neurodevelopment

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