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

Ville M. Koistinen, Olli Kärkkäinen, Klaudyna Borewicz, Iman Zarei, Jenna Jokkala, Valérie Micard, Natalia Rosa-Sibakov, Seppo Auriola, Anna Marja Aura, Hauke Smidt, Kati Hanhineva

Research output: Contribution to journalArticleScientificpeer-review

Abstract

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.

Original languageEnglish
Article number103
JournalMicrobiome
Volume7
Issue number1
DOIs
Publication statusPublished - 10 Jul 2019
MoE publication typeA1 Journal article-refereed

Fingerprint

Betaine
Fermentation
Diet
Microbiota
Ruminococcus
Bifidobacterium
Metabolomics
In Vitro Techniques
Gastrointestinal Microbiome
Dietary Fiber
Lactobacillus
Inbred C57BL Mouse
rRNA Genes
Health Status
Colon
Chronic Disease
Health

Keywords

  • Betaine
  • Bran
  • Colon model
  • Diet-microbiota interaction
  • Whole grain

Cite this

Koistinen, V. M., Kärkkäinen, O., Borewicz, K., Zarei, I., Jokkala, J., Micard, V., ... Hanhineva, K. (2019). Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation. Microbiome, 7(1), [103]. https://doi.org/10.1186/s40168-019-0718-2
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. In: Microbiome. 2019 ; Vol. 7, No. 1.
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abstract = "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.",
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Koistinen, VM, Kärkkäinen, O, Borewicz, K, Zarei, I, Jokkala, J, Micard, V, Rosa-Sibakov, N, Auriola, S, Aura, AM, Smidt, H & Hanhineva, K 2019, 'Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation', Microbiome, vol. 7, no. 1, 103. https://doi.org/10.1186/s40168-019-0718-2

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.

In: Microbiome, Vol. 7, No. 1, 103, 10.07.2019.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation

AU - Koistinen, Ville M.

AU - Kärkkäinen, Olli

AU - Borewicz, Klaudyna

AU - Zarei, Iman

AU - Jokkala, Jenna

AU - Micard, Valérie

AU - Rosa-Sibakov, Natalia

AU - Auriola, Seppo

AU - Aura, Anna Marja

AU - Smidt, Hauke

AU - Hanhineva, Kati

PY - 2019/7/10

Y1 - 2019/7/10

N2 - 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.

AB - 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.

KW - Betaine

KW - Bran

KW - Colon model

KW - Diet-microbiota interaction

KW - Whole grain

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U2 - 10.1186/s40168-019-0718-2

DO - 10.1186/s40168-019-0718-2

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