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

Pichler, Michael Jakob ; Yamada, Chihaya ; Shuoker, Bashar ; Alvarez-Silva, Camila ; Gotoh, Aina ; Leth, Maria Louise ; Schoof, Erwin ; Katoh, Toshihiko ; Sakanaka, Mikiyasu and Katayama, Takane , et al. (2020) In Nature Communications 11(1).
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... (More)

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.

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publishing date
type
Contribution to journal
publication status
published
subject
in
Nature Communications
volume
11
issue
1
article number
3285
publisher
Nature Publishing Group
external identifiers
  • scopus:85087393625
  • pmid:32620774
ISSN
2041-1723
DOI
10.1038/s41467-020-17075-x
language
English
LU publication?
no
id
f54d52bd-9dbc-43c1-9a9f-54038bba6ccd
date added to LUP
2020-12-22 12:46:05
date last changed
2024-06-28 06:56:17
@article{f54d52bd-9dbc-43c1-9a9f-54038bba6ccd,
  abstract     = {{<p>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.</p>}},
  author       = {{Pichler, Michael Jakob and Yamada, Chihaya and Shuoker, Bashar and Alvarez-Silva, Camila and Gotoh, Aina and Leth, Maria Louise and Schoof, Erwin and Katoh, Toshihiko and Sakanaka, Mikiyasu and Katayama, Takane and Jin, Chunsheng and Karlsson, Niclas G. and Arumugam, Manimozhiyan and Fushinobu, Shinya and Abou Hachem, Maher}},
  issn         = {{2041-1723}},
  language     = {{eng}},
  number       = {{1}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature Communications}},
  title        = {{Butyrate producing colonic Clostridiales metabolise human milk oligosaccharides and cross feed on mucin via conserved pathways}},
  url          = {{http://dx.doi.org/10.1038/s41467-020-17075-x}},
  doi          = {{10.1038/s41467-020-17075-x}},
  volume       = {{11}},
  year         = {{2020}},
}