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other·preclinical research, nutrition, biomedical research, gastroenterology, neurology·PMC10033698

Demonstrating a link between diet, gut microbiota and brain: 14 C radioactivity identified in the brain following gut microbial fermentation of 14 C-radiolabeled tyrosine in a pig model

Frontiers in Nutrition · 13 authors, 7 centres

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TL;DR

This preclinical study in weanling pigs developed a novel ^14C-radiolabeling workflow to trace nutrient metabolism. The central result was the detection of radioactivity from ^14C-tyrosine, delivered to a gut microbiota primed on a resistant protein diet, in the brain.

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This study used a novel ^14C-radiolabeling workflow in weanling pigs to investigate the biodistribution of nutrients metabolized by the gut microbiota. Male pigs were fed either a standard diet (^14C-ALA group) or a high resistant protein diet primed for gut fermentation (^14C-Tyr group). The key finding was that ^14C radioactivity from administered ^14C-tyrosine was detected in the brain, representing 0.15% of the original dose. The authors interpret this as evidence that metabolites from gut-fermented protein, such as tyrosine-derived compounds, are bioavailable to the brain. A major limitation is the lack of controls for ^14C-Tyr on a standard diet due to prohibitive costs, meaning the biodistribution specifically resulting from the resistant protein-primed microbiota cannot be compared to a normal diet. The study demonstrates a proof-of-concept pathway between diet, gut microbiota, and brain, but further research is needed to identify the specific compounds and their functional effects.

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other

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preclinical research

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ORIGINAL PAPER

PMC10033698

Demonstrating a link between diet, gut microbiota and brain: 14 C radioactivity identified in the brain following gut microbial fermentation of 14 C-radiolabeled tyrosine in a pig model

Frontiers in Nutrition

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ABSTRACT

Abstract Background There is a need to better understand the relationship between the diet, the gut microbiota and mental health. Metabolites produced when the human gut microbiota metabolize amino acids may enter the bloodstream and have systemic effects. We hypothesize that fermentation of amino acids by a resistant protein-primed gut microbiota could yield potentially toxic metabolites and disturb the availability of neurotransmitter precursors to the brain. However, these mechanisms are challenging to investigate via typical in vitro and clinical methods. Methods We developed a novel workflow using 14 C radiolabeling to investigate complex nutrient-disease relationships. The first three steps of the workflow are reported here. α-Linolenic acid (ALA) was used as a model nutrient to confirm the efficacy of the workflow, and tyrosine (Tyr) was the test nutrient. 14 C-Tyr was administered to male weanling pigs fed a high resistant protein diet, which primed the gut microbiota for fermenting protein. The hypotheses were; (1) that expected biodistribution of 14 C-ALA would be observed, and (2) that radioactivity from 14 C-Tyr, representing Tyr and other amino acids released from resistant protein following gut microbial fermentation, would be bioavailable to the brain. Results Radioactivity from the 14 C-ALA was detected in tissues reflecting normal utilization of this essential fatty acid. Radioactivity from the 14 C-Tyr was detected in the brain (0.15% of original dose). Conclusion Metabolites of gut-fermented protein and specifically amino acid precursors to neurotransmitters such as tyrosine, are potentially able to affect brain function. By extension, resistant proteins in the diet reaching the gut microbiota, also have potential to release metabolites that can potentially affect brain function. The high specificity of detection of 14 C radioactivity demonstrates that the proposed workflow can similarly be applied to understand other key diet and health paradigms. Keywords: biodistribution, tyrosine, resistant protein, α-linolenic acid, carbon-14 radio-isotope, gut-brain axis

CITATION EXPORT

Margaret Murray, Christopher K Barlow, Scott Blundell et al.. Demonstrating a link between diet, gut microbiota and brain: 14C radioactivity identified in the brain following gut microbial fermentation of 14C-radiolabeled tyrosine in a pig model. Frontiers in Nutrition. (2023). https://doi.org/10.3389/fnut.2023.1127729

AUTHORS

13 · 7 CENTRES

Margaret Murray, Christopher K Barlow, Scott Blundell, Mark Buecking, Anne Gibbon, Bernd Goeckener, Lisa M Kaminskas, Patricia Leitner, Sophie Selby-Pham, Andrew Sinclair, Habtewold D Waktola, Gary Williamson, Louise E Bennett

1School of Chemistry, Monash University, Clayton, VIC, Australia
2Department of Nutrition, Dietetics and Food, Monash University, Notting Hill, VIC, Australia
3Monash Proteomics and Metabolomics Facility and Monash Biomedicine Discovery Institute, Monash University, Clayton, VIC, Australia
4Fraunhofer Institute for Molecular Biology and Applied Ecology, Schmallenberg, Germany
5Monash Animal Research Platform, Monash University, Churchill, VIC, Australia
6School of Biomedical Sciences, Faculty of Medicine, The University of Queensland, Brisbane, QLD, Australia
7Faculty of Health Sciences, School of Pharmacy, Institute of Health, Jimma University, Jimma, Ethiopia

Margaret Murray, Christopher K Barlow, Scott Blundell et al.. Demonstrating a link between diet, gut microbiota and brain: 14C radioactivity identified in the brain following gut microbial fermentation of 14C-radiolabeled tyrosine in a pig model. Frontiers in Nutrition. (2023). https://doi.org/10.3389/fnut.2023.1127729