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Butyrate producing colonic Clostridiales metabolise human milk oligosaccharides and cross feed on mucin via conserved pathways

Author

Listed:
  • Michael Jakob Pichler

    (Technical University of Denmark)

  • Chihaya Yamada

    (The University of Tokyo)

  • Bashar Shuoker

    (Technical University of Denmark
    Lund University)

  • Camila Alvarez-Silva

    (University of Copenhagen)

  • Aina Gotoh

    (Kyoto University)

  • Maria Louise Leth

    (Technical University of Denmark)

  • Erwin Schoof

    (Technical University of Denmark)

  • Toshihiko Katoh

    (Kyoto University)

  • Mikiyasu Sakanaka

    (Ishikawa Prefectural University)

  • Takane Katayama

    (Kyoto University
    Ishikawa Prefectural University)

  • Chunsheng Jin

    (University of Gothenburg)

  • Niclas G. Karlsson

    (University of Gothenburg)

  • Manimozhiyan Arumugam

    (University of Copenhagen)

  • Shinya Fushinobu

    (The University of Tokyo)

  • Maher Abou Hachem

    (Technical University of Denmark)

Abstract

The early life human gut microbiota exerts life-long health effects on the host, but the mechanisms underpinning its assembly remain elusive. Particularly, the early colonization of Clostridiales from the Roseburia-Eubacterium group, associated with protection from colorectal cancer, immune- and metabolic disorders is enigmatic. Here, we describe catabolic pathways that support the growth of Roseburia and Eubacterium members on distinct human milk oligosaccharides (HMOs). The HMO pathways, which include enzymes with a previously unknown structural fold and specificity, were upregulated together with additional glycan-utilization loci during growth on selected HMOs and in co-cultures with Akkermansia muciniphila on mucin, suggesting an additional role in enabling cross-feeding and access to mucin O-glycans. Analyses of 4599 Roseburia genomes underscored the preponderance and diversity of the HMO utilization loci within the genus. The catabolism of HMOs by butyrate-producing Clostridiales may contribute to the competitiveness of this group during the weaning-triggered maturation of the microbiota.

Suggested Citation

  • Michael Jakob Pichler & Chihaya Yamada & Bashar Shuoker & Camila Alvarez-Silva & Aina Gotoh & Maria Louise Leth & Erwin Schoof & Toshihiko Katoh & Mikiyasu Sakanaka & Takane Katayama & Chunsheng Jin &, 2020. "Butyrate producing colonic Clostridiales metabolise human milk oligosaccharides and cross feed on mucin via conserved pathways," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17075-x
    DOI: 10.1038/s41467-020-17075-x
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    Cited by:

    1. Xiaoqian Lin & Tongyuan Hu & Jianwei Chen & Hewei Liang & Jianwei Zhou & Zhinan Wu & Chen Ye & Xin Jin & Xun Xu & Wenwei Zhang & Xiaohuan Jing & Tao Yang & Jian Wang & Huanming Yang & Karsten Kristian, 2023. "The genomic landscape of reference genomes of cultivated human gut bacteria," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Itxaso Anso & Andreas Naegeli & Javier O. Cifuente & Ane Orrantia & Erica Andersson & Olatz Zenarruzabeitia & Alicia Moraleda-Montoya & Mikel García-Alija & Francisco Corzana & Rafael A. Orbe & Franci, 2023. "Turning universal O into rare Bombay type blood," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Bashar Shuoker & Michael J. Pichler & Chunsheng Jin & Hiroka Sakanaka & Haiyang Wu & Ana Martínez Gascueña & Jining Liu & Tine Sofie Nielsen & Jan Holgersson & Eva Nordberg Karlsson & Nathalie Juge & , 2023. "Sialidases and fucosidases of Akkermansia muciniphila are crucial for growth on mucin and nutrient sharing with mucus-associated gut bacteria," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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