Metabolic impact of polyphenol-rich aronia fruit juice mediated by inflammation status of gut microbiome donors in humanized mouse model

Stephanie M G Wilson; Jesse T Peach; Hunter Fausset; Zachary T Miller; Seth T Walk; Carl J Yeoman; Brian Bothner; Mary P Miles

doi:10.3389/fnut.2023.1244692

Metabolic impact of polyphenol-rich aronia fruit juice mediated by inflammation status of gut microbiome donors in humanized mouse model

Front Nutr. 2023 Sep 1:10:1244692. doi: 10.3389/fnut.2023.1244692. eCollection 2023.

Authors

Stephanie M G Wilson¹, Jesse T Peach², Hunter Fausset², Zachary T Miller³, Seth T Walk⁴, Carl J Yeoman⁵, Brian Bothner², Mary P Miles¹

Affiliations

¹ Department of Food Systems, Nutrition, and Kinesiology, Montana State University, Bozeman, MT, United States.
² Department of Chemistry and Biochemistry, Montana State University, Bozeman, MT, United States.
³ Department of Research Centers, Montana State University, Bozeman, MT, United States.
⁴ Department of Microbiology and Cell Biology, Montana State University, Bozeman, MT, United States.
⁵ Department of Animal and Range Sciences, Montana State University, Bozeman, MT, United States.

Abstract

Background: The Aronia melanocarpa fruit is emerging as a health food owing to its high polyphenolic content and associated antioxidant activity. Antioxidant-rich foods, such as Aronia fruit, may counter inflammatory stimuli and positively modulate the gut microbiome. However, a comprehensive study characterizing the impact of Aronia fruit supplementation has not been completed. Therefore, we completed analyses measuring the metabolic, microbial, and inflammatory effects of a diet supplemented with Aronia fruit juice.

Method: Humanized mice were generated by colonizing gnotobiotic mice with microbiomes from human donors presenting disparate inflammation levels. Blood and fecal samples were collected throughout the course of an 8-week dietary intervention with either Aronia juice or a carbohydrate-matched beverage alone (2 weeks) or in combination with a high-fat diet to induce inflammation (6 weeks). Samples were analyzed using 16S rRNA gene sequencing (stool) and liquid chromatography-mass spectrometry (serum).

Results: We demonstrated transfer of microbiome composition and diversity and metabolic characteristics from humans with low and high inflammation levels to second-generation humanized mice. Aronia supplementation provided robust protection against high-fat diet induced metabolic and microbiome changes that were dependent in part on microbiome donor. Aronia induced increases in bacteria of the Eggerthellaceae genus (7-fold) which aligns with its known ability to metabolize (poly)phenols and in phosphatidylcholine metabolites which are consistent with improved gut barrier function. The gut microbiome from a low inflammation phenotype donor provided protection against high-fat diet induced loss of microbiome β-diversity and global metabolomic shifts compared to that from the high inflammation donor.

Conclusion: These metabolic changes elucidate pathway-specific drivers of reduced inflammation stemming from both Aronia and the gut microbiota.

Keywords: functional food; gastrointestinal microbiome; high fat diet; inflammation; metabolomics.