Vitamin A carotenoids, but not retinoids, mediate the impact of a healthy diet on gut microbial diversity

Valdes, Ana M.; Louca, Panayiotis; Visconti, Alessia; Asnicar, Francesco; Bermingham, Kate; Nogal, Ana; Wong, Kari; Michelotti, Gregory A.; Wolf, Jonathan; Segata, Nicola; Spector, Tim D.; Berry, Sarah E.; Falchi, Mario; Menni, Cristina

Abstract

: Background: Vitamin A is essential for physiological processes like vision and immunity. Vitamin A’s effect on gut microbiome composition, which affects absorption and metabolism of other vitamins, is still unknown. Here we examined the relationship between gut metagenome composition and six vitamin A-related metabolites (two retinoid: -retinol, 4 oxoretinoic acid (oxoRA) and four carotenoid metabolites, including beta-cryptoxanthin and three carotene diols). Methods: We included 1053 individuals from the TwinsUK cohort with vitamin A-related metabolites measured in serum and faeces, diet history, and gut microbiome composition assessed by shotgun metagenome sequencing. Results were replicated in 327 women from the ZOE PREDICT-1 study. Results: Five vitamin A-related serum metabolites were positively correlated with microbiome alpha diversity (r = 0.15 to r = 0.20, p < 4 × 10−6). Carotenoid compounds were positively correlated with the short-chain fatty-acid-producing bacteria Faecalibacterium prausnitzii and Coprococcus eutactus. Retinol was not associated with any microbial species. We found that gut microbiome composition could predict circulating levels of carotenoids and oxoretinoic acid with AUCs ranging from 0.66 to 0.74 using random forest models, but not retinol (AUC = 0.52). The healthy eating index (HEI) was strongly associated with gut microbiome diversity and with all carotenoid compounds, but not retinoids. We investigated the mediating role of carotenoid compounds on the effect of a healthy diet (HEI) on gut microbiome diversity, finding that carotenoids significantly mediated between 18 and 25% of the effect of HEI on gut microbiome alpha diversity. Conclusions: Our results show strong links between circulating carotene compounds and gut microbiome composition and potential links to a healthy diet pattern.

Citation

Valdes, A. M., Louca, P., Visconti, A., Asnicar, F., Bermingham, K., Nogal, A., Wong, K., Michelotti, G. A., Wolf, J., Segata, N., Spector, T. D., Berry, S. E., Falchi, M., & Menni, C. (2024). Vitamin A carotenoids, but not retinoids, mediate the impact of a healthy diet on gut microbial diversity. BMC Medicine, 22, Article 321. https://doi.org/10.1186/s12916-024-03543-4

• Journal Article Type: Article
• Acceptance Date: Jul 28, 2024
• Online Publication Date: Aug 7, 2024
• Publication Date: Aug 7, 2024
• Deposit Date: Oct 14, 2024
• Publicly Available Date: Oct 15, 2024
• Journal: BMC Medicine
• Electronic ISSN: 1741-7015
• Publisher: Springer Verlag
• Peer Reviewed: Peer Reviewed
• Volume: 22
• Article Number: 321
• DOI: https://doi.org/10.1186/s12916-024-03543-4
• Keywords: Carotenoids, Gut microbiome composition, Vitamin A metabolites, Retinoids
• Public URL: https://nottingham-repository.worktribe.com/output/38365953
• Publisher URL: https://link.springer.com/article/10.1186/s12916-024-03543-4