Cooperative action of gut-microbiota-accessible carbohydrates improves host metabolic function

Sawako Tomioka; Natsumi Seki; Yuki Sugiura; Masahiro Akiyama; Jun Uchiyama; Genki Yamaguchi; Kyosuke Yakabe; Ryuta Ejima; Kouya Hattori; Tatsuki Kimizuka; Yumiko Fujimura; Hiroki Sato; Monica Gondo; Satoru Ozaki; Yoshiko Honme; Makoto Suematsu; Ikuo Kimura; Naohiro Inohara; Gabriel Núñez; Koji Hase; Yun Gi Kim

doi:10.1016/j.celrep.2022.111087

Cooperative action of gut-microbiota-accessible carbohydrates improves host metabolic function

Sawako Tomioka, Natsumi Seki, Yuki Sugiura, Masahiro Akiyama, Jun Uchiyama, Genki Yamaguchi, Kyosuke Yakabe, Ryuta Ejima, Kouya Hattori, Tatsuki Kimizuka, Yumiko Fujimura, Hiroki Sato, Monica Gondo, Satoru Ozaki, Yoshiko Honme, Makoto Suematsu, Ikuo Kimura, Naohiro Inohara, Gabriel Núñez, Koji HaseYun Gi Kim

Research output: Contribution to journal › Article › peer-review

9 Citations (Scopus)

Abstract

Microbiota-accessible carbohydrates (MACs) exert health-promoting effects, but how each MAC impacts gut microbiota and regulates host physiology remains unclear. Here, we show that L-arabinose and sucrose cooperatively act on gut microbiota and exert anti-obesogenic effects. Specifically, L-arabinose, a monosaccharide that is poorly absorbed in the gut and inhibits intestinal sucrase, suppresses diet-induced obesity in mice in the presence of sucrose. Additionally, the suppressive effect of L-arabinose on adiposity is abrogated in mice lacking the short-chain fatty acid (SCFA) receptors GPR43 and GPR41. Mechanistically, L-arabinose increases the relative abundance of acetate and propionate producers (e.g., Bacteroides), while sucrose enhances SCFA production. Furthermore, L-arabinose and sucrose activate the glycolytic and pentose phosphate pathways of Bacteroides, respectively, indicating that they synergistically promote acetate production through distinct pathways. These findings suggest that each MAC has a unique property and thus may serve as a precision gut-microbiota modulator to promote host homeostasis.

Original language	English
Article number	111087
Journal	Cell Reports
Volume	40
Issue number	3
DOIs	https://doi.org/10.1016/j.celrep.2022.111087
Publication status	Published - 2022 Jul 19

Keywords

CP: Microbiology
L-arabinose
gut microbiota
metabolism
microbiota-accessible carbohydrates
obesity
short-chain fatty acids
sucrose

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.celrep.2022.111087

Cite this

Tomioka, S., Seki, N., Sugiura, Y., Akiyama, M., Uchiyama, J., Yamaguchi, G., Yakabe, K., Ejima, R., Hattori, K., Kimizuka, T., Fujimura, Y., Sato, H., Gondo, M., Ozaki, S., Honme, Y., Suematsu, M., Kimura, I., Inohara, N., Núñez, G., ... Kim, Y. G. (2022). Cooperative action of gut-microbiota-accessible carbohydrates improves host metabolic function. Cell Reports, 40(3), Article 111087. https://doi.org/10.1016/j.celrep.2022.111087

Tomioka, S, Seki, N, Sugiura, Y, Akiyama, M, Uchiyama, J, Yamaguchi, G, Yakabe, K, Ejima, R, Hattori, K, Kimizuka, T, Fujimura, Y, Sato, H, Gondo, M, Ozaki, S, Honme, Y, Suematsu, M, Kimura, I, Inohara, N, Núñez, G, Hase, K & Kim, YG 2022, 'Cooperative action of gut-microbiota-accessible carbohydrates improves host metabolic function', Cell Reports, vol. 40, no. 3, 111087. https://doi.org/10.1016/j.celrep.2022.111087

@article{2e08b868d4814eee8ab96879ccdd6805,

title = "Cooperative action of gut-microbiota-accessible carbohydrates improves host metabolic function",

abstract = "Microbiota-accessible carbohydrates (MACs) exert health-promoting effects, but how each MAC impacts gut microbiota and regulates host physiology remains unclear. Here, we show that L-arabinose and sucrose cooperatively act on gut microbiota and exert anti-obesogenic effects. Specifically, L-arabinose, a monosaccharide that is poorly absorbed in the gut and inhibits intestinal sucrase, suppresses diet-induced obesity in mice in the presence of sucrose. Additionally, the suppressive effect of L-arabinose on adiposity is abrogated in mice lacking the short-chain fatty acid (SCFA) receptors GPR43 and GPR41. Mechanistically, L-arabinose increases the relative abundance of acetate and propionate producers (e.g., Bacteroides), while sucrose enhances SCFA production. Furthermore, L-arabinose and sucrose activate the glycolytic and pentose phosphate pathways of Bacteroides, respectively, indicating that they synergistically promote acetate production through distinct pathways. These findings suggest that each MAC has a unique property and thus may serve as a precision gut-microbiota modulator to promote host homeostasis.",

keywords = "CP: Microbiology, L-arabinose, gut microbiota, metabolism, microbiota-accessible carbohydrates, obesity, short-chain fatty acids, sucrose",

author = "Sawako Tomioka and Natsumi Seki and Yuki Sugiura and Masahiro Akiyama and Jun Uchiyama and Genki Yamaguchi and Kyosuke Yakabe and Ryuta Ejima and Kouya Hattori and Tatsuki Kimizuka and Yumiko Fujimura and Hiroki Sato and Monica Gondo and Satoru Ozaki and Yoshiko Honme and Makoto Suematsu and Ikuo Kimura and Naohiro Inohara and Gabriel N{\'u}{\~n}ez and Koji Hase and Kim, {Yun Gi}",

note = "Funding Information: This work was supported by research grants from the JSPS KAKENHI (JP17H05068 and JP20H03490 to Y.-G.K.), AMED (JP18gm6010004h0003 to Y.-G.K.), Takeda Science Foundation (to Y.-G.K.), the Naito Foundation (to Y.-G.K.), Yakult Bio-Science Foundation (to Y.-G.K.), and Mochida Memorial Foundation for Medical and Pharmaceutical Research (to Y.-G.K.). Y.-G.K. conceived the study and designed the experiments; S.T. N.S. Y.S. M.A. J.U. G.Y. K.Y. R.E. K. Hattori, T.K. H.S. M.G. S.O. Y.H. and Y.-G.K. collected samples and conducted the experiments; Y.F. I.K. and K. Hase provided mouse strains; S.T. N.S. Y.S. M.A. J.U. G.Y. K.Y. K. Hattori, T.K. S.O. M.S. N.I. and Y.-G.K. analyzed data; S.T. N.S. G.N. and Y.-G.K. prepared the manuscript. Y.-G.K. supervised the project. All authors read and approved the final manuscript. S.O. and Y.H. are employees of Co-Creation Center, Meiji Holdings Co. Ltd. Funding Information: This work was supported by research grants from the JSPS KAKENHI ( JP17H05068 and JP20H03490 to Y.-G.K.), AMED ( JP18gm6010004h0003 to Y.-G.K.), Takeda Science Foundation (to Y.-G.K.), the Naito Foundation (to Y.-G.K.), Yakult Bio-Science Foundation (to Y.-G.K.), and Mochida Memorial Foundation for Medical and Pharmaceutical Research (to Y.-G.K.). Publisher Copyright: {\textcopyright} 2022 The Author(s)",

year = "2022",

month = jul,

day = "19",

doi = "10.1016/j.celrep.2022.111087",

language = "English",

volume = "40",

journal = "Cell Reports",

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TY - JOUR

T1 - Cooperative action of gut-microbiota-accessible carbohydrates improves host metabolic function

AU - Tomioka, Sawako

AU - Seki, Natsumi

AU - Sugiura, Yuki

AU - Akiyama, Masahiro

AU - Uchiyama, Jun

AU - Yamaguchi, Genki

AU - Yakabe, Kyosuke

AU - Ejima, Ryuta

AU - Hattori, Kouya

AU - Kimizuka, Tatsuki

AU - Fujimura, Yumiko

AU - Sato, Hiroki

AU - Gondo, Monica

AU - Ozaki, Satoru

AU - Honme, Yoshiko

AU - Suematsu, Makoto

AU - Kimura, Ikuo

AU - Inohara, Naohiro

AU - Núñez, Gabriel

AU - Hase, Koji

AU - Kim, Yun Gi

N1 - Funding Information: This work was supported by research grants from the JSPS KAKENHI (JP17H05068 and JP20H03490 to Y.-G.K.), AMED (JP18gm6010004h0003 to Y.-G.K.), Takeda Science Foundation (to Y.-G.K.), the Naito Foundation (to Y.-G.K.), Yakult Bio-Science Foundation (to Y.-G.K.), and Mochida Memorial Foundation for Medical and Pharmaceutical Research (to Y.-G.K.). Y.-G.K. conceived the study and designed the experiments; S.T. N.S. Y.S. M.A. J.U. G.Y. K.Y. R.E. K. Hattori, T.K. H.S. M.G. S.O. Y.H. and Y.-G.K. collected samples and conducted the experiments; Y.F. I.K. and K. Hase provided mouse strains; S.T. N.S. Y.S. M.A. J.U. G.Y. K.Y. K. Hattori, T.K. S.O. M.S. N.I. and Y.-G.K. analyzed data; S.T. N.S. G.N. and Y.-G.K. prepared the manuscript. Y.-G.K. supervised the project. All authors read and approved the final manuscript. S.O. and Y.H. are employees of Co-Creation Center, Meiji Holdings Co. Ltd. Funding Information: This work was supported by research grants from the JSPS KAKENHI ( JP17H05068 and JP20H03490 to Y.-G.K.), AMED ( JP18gm6010004h0003 to Y.-G.K.), Takeda Science Foundation (to Y.-G.K.), the Naito Foundation (to Y.-G.K.), Yakult Bio-Science Foundation (to Y.-G.K.), and Mochida Memorial Foundation for Medical and Pharmaceutical Research (to Y.-G.K.). Publisher Copyright: © 2022 The Author(s)

PY - 2022/7/19

Y1 - 2022/7/19

N2 - Microbiota-accessible carbohydrates (MACs) exert health-promoting effects, but how each MAC impacts gut microbiota and regulates host physiology remains unclear. Here, we show that L-arabinose and sucrose cooperatively act on gut microbiota and exert anti-obesogenic effects. Specifically, L-arabinose, a monosaccharide that is poorly absorbed in the gut and inhibits intestinal sucrase, suppresses diet-induced obesity in mice in the presence of sucrose. Additionally, the suppressive effect of L-arabinose on adiposity is abrogated in mice lacking the short-chain fatty acid (SCFA) receptors GPR43 and GPR41. Mechanistically, L-arabinose increases the relative abundance of acetate and propionate producers (e.g., Bacteroides), while sucrose enhances SCFA production. Furthermore, L-arabinose and sucrose activate the glycolytic and pentose phosphate pathways of Bacteroides, respectively, indicating that they synergistically promote acetate production through distinct pathways. These findings suggest that each MAC has a unique property and thus may serve as a precision gut-microbiota modulator to promote host homeostasis.

AB - Microbiota-accessible carbohydrates (MACs) exert health-promoting effects, but how each MAC impacts gut microbiota and regulates host physiology remains unclear. Here, we show that L-arabinose and sucrose cooperatively act on gut microbiota and exert anti-obesogenic effects. Specifically, L-arabinose, a monosaccharide that is poorly absorbed in the gut and inhibits intestinal sucrase, suppresses diet-induced obesity in mice in the presence of sucrose. Additionally, the suppressive effect of L-arabinose on adiposity is abrogated in mice lacking the short-chain fatty acid (SCFA) receptors GPR43 and GPR41. Mechanistically, L-arabinose increases the relative abundance of acetate and propionate producers (e.g., Bacteroides), while sucrose enhances SCFA production. Furthermore, L-arabinose and sucrose activate the glycolytic and pentose phosphate pathways of Bacteroides, respectively, indicating that they synergistically promote acetate production through distinct pathways. These findings suggest that each MAC has a unique property and thus may serve as a precision gut-microbiota modulator to promote host homeostasis.

KW - CP: Microbiology

KW - L-arabinose

KW - gut microbiota

KW - metabolism

KW - microbiota-accessible carbohydrates

KW - obesity

KW - short-chain fatty acids

KW - sucrose

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DO - 10.1016/j.celrep.2022.111087

M3 - Article

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AN - SCOPUS:85134777535

SN - 2211-1247

VL - 40

JO - Cell Reports

JF - Cell Reports

IS - 3

M1 - 111087

ER -

Cooperative action of gut-microbiota-accessible carbohydrates improves host metabolic function

Abstract

Keywords

ASJC Scopus subject areas

UN SDGs

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