Cargando…

Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation

BACKGROUND: Accumulating evidence is supporting the protective effect of whole grains against several chronic diseases. Simultaneously, our knowledge is increasing on the impact of gut microbiota on our health and on how diet can modify the composition of our bacterial cohabitants. Herein, we studie...

Descripción completa

Detalles Bibliográficos
Autores principales: Koistinen, Ville M., Kärkkäinen, Olli, Borewicz, Klaudyna, Zarei, Iman, Jokkala, Jenna, Micard, Valérie, Rosa-Sibakov, Natalia, Auriola, Seppo, Aura, Anna-Marja, Smidt, Hauke, Hanhineva, Kati
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6621954/
https://www.ncbi.nlm.nih.gov/pubmed/31291994
http://dx.doi.org/10.1186/s40168-019-0718-2
_version_ 1783434138852786176
author Koistinen, Ville M.
Kärkkäinen, Olli
Borewicz, Klaudyna
Zarei, Iman
Jokkala, Jenna
Micard, Valérie
Rosa-Sibakov, Natalia
Auriola, Seppo
Aura, Anna-Marja
Smidt, Hauke
Hanhineva, Kati
author_facet Koistinen, Ville M.
Kärkkäinen, Olli
Borewicz, Klaudyna
Zarei, Iman
Jokkala, Jenna
Micard, Valérie
Rosa-Sibakov, Natalia
Auriola, Seppo
Aura, Anna-Marja
Smidt, Hauke
Hanhineva, Kati
author_sort Koistinen, Ville M.
collection PubMed
description BACKGROUND: Accumulating evidence is supporting the protective effect of whole grains against several chronic diseases. Simultaneously, our knowledge is increasing on the impact of gut microbiota on our health and on how diet can modify the composition of our bacterial cohabitants. Herein, we studied C57BL/6 J mice fed with diets enriched with rye bran and wheat aleurone, conventional and germ-free C57BL/6NTac mice on a basal diet, and the colonic fermentation of rye bran in an in vitro model of the human gastrointestinal system. We performed 16S rRNA gene sequencing and metabolomics on the study samples to determine the effect of bran-enriched diets on the gut microbial composition and the potential contribution of microbiota to the metabolism of a novel group of betainized compounds. RESULTS: The bran-enriched study diets elevated the levels of betainized compounds in the colon contents of C57BL/6 J mice. The composition of microbiota changed, and the bran-enriched diets induced an increase in the relative abundance of several bacterial taxa, including Akkermansia, Bifidobacterium, Coriobacteriaceae, Lactobacillus, Parasutterella, and Ruminococcus, many of which are associated with improved health status or the metabolism of plant-based molecules. The levels of betainized compounds in the gut tissues of germ-free mice were significantly lower compared to conventional mice. In the in vitro model of the human gut, the production of betainized compounds was observed throughout the incubation, while the levels of glycine betaine decreased. In cereal samples, only low levels or trace amounts of other betaines than glycine betaine were observed. CONCLUSIONS: Our findings provide evidence that the bacterial taxa increased in relative abundance by the bran-based diet are also involved in the metabolism of glycine betaine into other betainized compounds, adding another potential compound group acting as a mediator of the synergistic metabolic effect of diet and colonic microbiota. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0718-2) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6621954
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-66219542019-07-22 Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation Koistinen, Ville M. Kärkkäinen, Olli Borewicz, Klaudyna Zarei, Iman Jokkala, Jenna Micard, Valérie Rosa-Sibakov, Natalia Auriola, Seppo Aura, Anna-Marja Smidt, Hauke Hanhineva, Kati Microbiome Research BACKGROUND: Accumulating evidence is supporting the protective effect of whole grains against several chronic diseases. Simultaneously, our knowledge is increasing on the impact of gut microbiota on our health and on how diet can modify the composition of our bacterial cohabitants. Herein, we studied C57BL/6 J mice fed with diets enriched with rye bran and wheat aleurone, conventional and germ-free C57BL/6NTac mice on a basal diet, and the colonic fermentation of rye bran in an in vitro model of the human gastrointestinal system. We performed 16S rRNA gene sequencing and metabolomics on the study samples to determine the effect of bran-enriched diets on the gut microbial composition and the potential contribution of microbiota to the metabolism of a novel group of betainized compounds. RESULTS: The bran-enriched study diets elevated the levels of betainized compounds in the colon contents of C57BL/6 J mice. The composition of microbiota changed, and the bran-enriched diets induced an increase in the relative abundance of several bacterial taxa, including Akkermansia, Bifidobacterium, Coriobacteriaceae, Lactobacillus, Parasutterella, and Ruminococcus, many of which are associated with improved health status or the metabolism of plant-based molecules. The levels of betainized compounds in the gut tissues of germ-free mice were significantly lower compared to conventional mice. In the in vitro model of the human gut, the production of betainized compounds was observed throughout the incubation, while the levels of glycine betaine decreased. In cereal samples, only low levels or trace amounts of other betaines than glycine betaine were observed. CONCLUSIONS: Our findings provide evidence that the bacterial taxa increased in relative abundance by the bran-based diet are also involved in the metabolism of glycine betaine into other betainized compounds, adding another potential compound group acting as a mediator of the synergistic metabolic effect of diet and colonic microbiota. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0718-2) contains supplementary material, which is available to authorized users. BioMed Central 2019-07-10 /pmc/articles/PMC6621954/ /pubmed/31291994 http://dx.doi.org/10.1186/s40168-019-0718-2 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Koistinen, Ville M.
Kärkkäinen, Olli
Borewicz, Klaudyna
Zarei, Iman
Jokkala, Jenna
Micard, Valérie
Rosa-Sibakov, Natalia
Auriola, Seppo
Aura, Anna-Marja
Smidt, Hauke
Hanhineva, Kati
Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation
title Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation
title_full Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation
title_fullStr Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation
title_full_unstemmed Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation
title_short Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation
title_sort contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6621954/
https://www.ncbi.nlm.nih.gov/pubmed/31291994
http://dx.doi.org/10.1186/s40168-019-0718-2
work_keys_str_mv AT koistinenvillem contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT karkkainenolli contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT borewiczklaudyna contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT zareiiman contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT jokkalajenna contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT micardvalerie contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT rosasibakovnatalia contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT auriolaseppo contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT auraannamarja contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT smidthauke contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation
AT hanhinevakati contributionofgutmicrobiotatometabolismofdietaryglycinebetaineinmiceandinvitrocolonicfermentation