Human gut microbiota and their production of endocannabinoid-like mediators are directly affected by a dietary oil

ABSTRACT

Dietary omega-3 polyunsaturated fatty acids (n-3 PUFAs) and the gut microbiome affect each other. We investigated the impact of supplementation with Buglossoides arvensis oil (BO), rich in stearidonic acid (SDA), on the human gut microbiome. Employing the Mucosal Simulator of the Human Intestinal Microbial Ecosystem (M-SHIME), we simulated the ileal and ascending colon microbiomes of four donors. Our results reveal two distinct microbiota clusters influenced by BO, exhibiting shared and contrasting shifts. Notably, Bacteroides and Clostridia abundance underwent similar changes in both clusters, accompanied by increased propionate production in the colon. However, in the ileum, cluster 2 displayed a higher metabolic activity in terms of BO-induced propionate levels. Accordingly, a triad of bacterial members involved in propionate production through the succinate pathway, namely Bacteroides, Parabacteroides, and Phascolarctobacterium, was identified particularly in this cluster, which also showed a surge of second-generation probiotics, such as Akkermansia, in the colon. Finally, we describe for the first time the capability of gut bacteria to produce N-acyl-ethanolamines, and particularly the SDA-derived N-stearidonoyl-ethanolamine, following BO supplementation, which also stimulated the production of another bioactive endocannabinoid-like molecule, commendamide, in both cases with variations across individuals. Spearman correlations enabled the identification of bacterial genera potentially involved in endocannabinoid-like molecule production, such as, in agreement with previous reports, Bacteroides in the case of commendamide. This study suggests that the potential health benefits on the human microbiome of certain dietary oils may be amenable to stratified nutrition strategies and extend beyond n-3 PUFAs to include microbiota-derived endocannabinoid-like mediators.

KEYWORDS:

• N-3 PUFAs
• Buglossoides arvensis
• Ahiflower
• plant-based oils
• SDA
• gut bacterial microbiota
• prebiotics
• lipid biotransformation
• M-SHIME® fermentation system
• commendamide
• endocannabinoids

Acknowledgments

The authors are grateful to INAF analytical and metabolomic platforms and would like to acknowledge Pier-Luc Plante for injecting the lipid compounds, and Roxanne Nolet and Perrine Feutry for their assistance in SCFAs measurements. We are also grateful to Elizabeth Dumais for providing an updated procedure of the lipid extraction and calibration. Finally, we thank Joseph Lupien-Meilleur for his help in creating the figure of the study design.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Authors’ contributions

C.R., C.S., and V.D. had full access to all the data in the study and accept the responsibility for the integrity of the data and the accuracy of the data analyses. C.R., C.S., and V.D. designed the study. C.S. and V.D. supervised the work. C.R., and P.G. conducted the in vitro fermentations and quality control. C.R. conducted the molecular-based experiments, and metagenomics sequencing. N.F. and J.L.L. conducted the lipidomics analysis. J.L.L. conducted the mathematical modeling. O.A. and N.F. developed and employed the commendamide analytical method. R.V. conducted the chemical synthesis of commendamide and its analogues in deuterated and non-deuterated forms. C.R. and M.S. performed the bioinformatics and data analysis. C.R. interpreted the overall data and wrote the manuscript first draft. C.R., C.S., V.D., N.F., F.R. and J.L.L. revised the manuscript.

Availability of data and materials

All data generated or analyzed during this study are included in this published article (and its supplementary information files). All 16S rRNA gene amplicon sequencing data were deposited in the Sequence Read Archive (SRA) under the BioProject PRJNA836582.

Ethics approval

Consent for fecal donation was obtained under registration number 2022–382/17-11-2022 (Laval University, Québec, Canada).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2024.2335879

Additional information

Funding

This work was supported by the Canada Research Excellence Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health (CERC-MEND), which is funded by the Tri-Agency of the Canadian Federal Government (The Canadian Institutes of Health Research (CIHR), the Natural Sciences and Engineering Research Council of Canada (NSERC), and the Social Sciences and Humanities Research Council of Canada (SSHRC)). Also supported by the International Joint Research Unit for Chemical and Biomolecular Research of the Microbiome and its Impact on Metabolic Health and Nutrition (UMI-MicroMeNu to V.D.), which is partly funded by the Apogée/Canada First programme of the Tri-Agency of the Canadian Federal Government, is also acknowledged.