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Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract

Dietary carbohydrates impact the composition of the human gut microbiota. However, the relationship between carbohydrate availability for individual bacteria and their growth in the intestinal environment remains unclear. Here, we show that the availability of long-chain xylans (LCX), one of the mos...

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Autores principales: Watanabe, Yohei, Saito, Yuki, Hara, Taeko, Tsukuda, Naoki, Aiyama-Suzuki, Yoshimi, Tanigawa-Yahagi, Kana, Kurakawa, Takashi, Moriyama-Ohara, Kaoru, Matsumoto, Satoshi, Matsuki, Takahiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723692/
https://www.ncbi.nlm.nih.gov/pubmed/37938239
http://dx.doi.org/10.1038/s43705-021-00066-4
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author Watanabe, Yohei
Saito, Yuki
Hara, Taeko
Tsukuda, Naoki
Aiyama-Suzuki, Yoshimi
Tanigawa-Yahagi, Kana
Kurakawa, Takashi
Moriyama-Ohara, Kaoru
Matsumoto, Satoshi
Matsuki, Takahiro
author_facet Watanabe, Yohei
Saito, Yuki
Hara, Taeko
Tsukuda, Naoki
Aiyama-Suzuki, Yoshimi
Tanigawa-Yahagi, Kana
Kurakawa, Takashi
Moriyama-Ohara, Kaoru
Matsumoto, Satoshi
Matsuki, Takahiro
author_sort Watanabe, Yohei
collection PubMed
description Dietary carbohydrates impact the composition of the human gut microbiota. However, the relationship between carbohydrate availability for individual bacteria and their growth in the intestinal environment remains unclear. Here, we show that the availability of long-chain xylans (LCX), one of the most abundant dietary fibres in the human diet, promotes the growth of Bifidobacterium pseudocatenulatum in the adult human gut. Genomic and phenotypic analyses revealed that the availability of LCX-derived oligosaccharides is a fundamental feature of B. pseudocatenulatum, and that some but not all strains possessing the endo-1,4-β-xylanase (BpXyn10A) gene grow on LCX by cleaving the xylose backbone. The BpXyn10A gene, likely acquired by horizontal transfer, was incorporated into the gene cluster for LCX-derived oligosaccharide utilisation. Co-culturing with xylanolytic Bacteroides spp. demonstrated that LCX-utilising strains are more competitive than LCX non-utilising strains even when LCX-derived oligosaccharides were supplied. In LCX-rich dietary interventions in adult humans, levels of endogenous B. pseudocatenulatum increased only when BpXyn10A was detected, indicating that LCX availability is a fitness determinant in the human gut. Our findings highlight the enhanced intestinal adaptability of bifidobacteria via polysaccharide utilisation, and provide a cornerstone for systematic manipulation of the intestinal microbiota through dietary intervention using key enzymes that degrade polysaccharide as biomarkers.
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spelling pubmed-97236922023-01-04 Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract Watanabe, Yohei Saito, Yuki Hara, Taeko Tsukuda, Naoki Aiyama-Suzuki, Yoshimi Tanigawa-Yahagi, Kana Kurakawa, Takashi Moriyama-Ohara, Kaoru Matsumoto, Satoshi Matsuki, Takahiro ISME Commun Article Dietary carbohydrates impact the composition of the human gut microbiota. However, the relationship between carbohydrate availability for individual bacteria and their growth in the intestinal environment remains unclear. Here, we show that the availability of long-chain xylans (LCX), one of the most abundant dietary fibres in the human diet, promotes the growth of Bifidobacterium pseudocatenulatum in the adult human gut. Genomic and phenotypic analyses revealed that the availability of LCX-derived oligosaccharides is a fundamental feature of B. pseudocatenulatum, and that some but not all strains possessing the endo-1,4-β-xylanase (BpXyn10A) gene grow on LCX by cleaving the xylose backbone. The BpXyn10A gene, likely acquired by horizontal transfer, was incorporated into the gene cluster for LCX-derived oligosaccharide utilisation. Co-culturing with xylanolytic Bacteroides spp. demonstrated that LCX-utilising strains are more competitive than LCX non-utilising strains even when LCX-derived oligosaccharides were supplied. In LCX-rich dietary interventions in adult humans, levels of endogenous B. pseudocatenulatum increased only when BpXyn10A was detected, indicating that LCX availability is a fitness determinant in the human gut. Our findings highlight the enhanced intestinal adaptability of bifidobacteria via polysaccharide utilisation, and provide a cornerstone for systematic manipulation of the intestinal microbiota through dietary intervention using key enzymes that degrade polysaccharide as biomarkers. Nature Publishing Group UK 2021-10-28 /pmc/articles/PMC9723692/ /pubmed/37938239 http://dx.doi.org/10.1038/s43705-021-00066-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Watanabe, Yohei
Saito, Yuki
Hara, Taeko
Tsukuda, Naoki
Aiyama-Suzuki, Yoshimi
Tanigawa-Yahagi, Kana
Kurakawa, Takashi
Moriyama-Ohara, Kaoru
Matsumoto, Satoshi
Matsuki, Takahiro
Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract
title Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract
title_full Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract
title_fullStr Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract
title_full_unstemmed Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract
title_short Xylan utilisation promotes adaptation of Bifidobacterium pseudocatenulatum to the human gastrointestinal tract
title_sort xylan utilisation promotes adaptation of bifidobacterium pseudocatenulatum to the human gastrointestinal tract
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723692/
https://www.ncbi.nlm.nih.gov/pubmed/37938239
http://dx.doi.org/10.1038/s43705-021-00066-4
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