Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut

Maria Louise Leth, Morten Ejby, Christopher Workman, David Adrian Ewald, Signe Schultz Pedersen, Claus Sternberg, Martin Iain Bahl, Tine Rask Licht, Finn Lillelund Aachmann, Bjørge Westereng, Maher Abou Hachem*

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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Abstract

Metabolism of dietary glycans is pivotal in shaping the human gut microbiota. However, the mechanisms that promote competition for glycans among gut commensals remain unclear. Roseburia intestinalis, an abundant butyrate-producing Firmicute, is a key degrader of the major dietary fibre xylan. Despite the association of this taxon to a healthy microbiota, insight is lacking into its glycan utilization machinery. Here, we investigate the apparatus that confers R. intestinalis growth on different xylans. R. intestinalis displays a large cell-attached modular xylanase that promotes multivalent and dynamic association to xylan via four xylan-binding modules. This xylanase operates in concert with an ATP-binding cassette transporter to mediate breakdown and selective internalization of xylan fragments. The transport protein of R. intestinalis prefers oligomers of 4-5 xylosyl units, whereas the counterpart from a model xylan-degrading Bacteroides commensal targets larger ligands. Although R. intestinalis and the Bacteroides competitor co-grew in a mixed culture on xylan, R. intestinalis dominated on the preferred transport substrate xylotetraose. These findings highlight the differentiation of capture and transport preferences as a possible strategy to facilitate co-growth on abundant dietary fibres and may offer a unique route to manipulate the microbiota based on glycan transport preferences in therapeutic interventions to boost distinct taxa.
Original languageEnglish
JournalNature Microbiology
Number of pages13
ISSN2058-5276
DOIs
Publication statusPublished - 2018

Cite this

@article{ebea4f85c726415c957ba36a3c7fcb9c,
title = "Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut",
abstract = "Metabolism of dietary glycans is pivotal in shaping the human gut microbiota. However, the mechanisms that promote competition for glycans among gut commensals remain unclear. Roseburia intestinalis, an abundant butyrate-producing Firmicute, is a key degrader of the major dietary fibre xylan. Despite the association of this taxon to a healthy microbiota, insight is lacking into its glycan utilization machinery. Here, we investigate the apparatus that confers R. intestinalis growth on different xylans. R. intestinalis displays a large cell-attached modular xylanase that promotes multivalent and dynamic association to xylan via four xylan-binding modules. This xylanase operates in concert with an ATP-binding cassette transporter to mediate breakdown and selective internalization of xylan fragments. The transport protein of R. intestinalis prefers oligomers of 4-5 xylosyl units, whereas the counterpart from a model xylan-degrading Bacteroides commensal targets larger ligands. Although R. intestinalis and the Bacteroides competitor co-grew in a mixed culture on xylan, R. intestinalis dominated on the preferred transport substrate xylotetraose. These findings highlight the differentiation of capture and transport preferences as a possible strategy to facilitate co-growth on abundant dietary fibres and may offer a unique route to manipulate the microbiota based on glycan transport preferences in therapeutic interventions to boost distinct taxa.",
author = "Leth, {Maria Louise} and Morten Ejby and Christopher Workman and Ewald, {David Adrian} and Pedersen, {Signe Schultz} and Claus Sternberg and Bahl, {Martin Iain} and Licht, {Tine Rask} and Aachmann, {Finn Lillelund} and Bj{\o}rge Westereng and {Abou Hachem}, Maher",
year = "2018",
doi = "10.1038/s41564-018-0132-8",
language = "English",
journal = "Nature Microbiology",
issn = "2058-5276",
publisher = "Nature Publishing Group",

}

Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut. / Leth, Maria Louise; Ejby, Morten; Workman, Christopher; Ewald, David Adrian; Pedersen, Signe Schultz; Sternberg, Claus; Bahl, Martin Iain; Licht, Tine Rask; Aachmann, Finn Lillelund; Westereng, Bjørge; Abou Hachem, Maher .

In: Nature Microbiology, 2018.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Differential bacterial capture and transport preferences facilitate co-growth on dietary xylan in the human gut

AU - Leth, Maria Louise

AU - Ejby, Morten

AU - Workman, Christopher

AU - Ewald, David Adrian

AU - Pedersen, Signe Schultz

AU - Sternberg, Claus

AU - Bahl, Martin Iain

AU - Licht, Tine Rask

AU - Aachmann, Finn Lillelund

AU - Westereng, Bjørge

AU - Abou Hachem, Maher

PY - 2018

Y1 - 2018

N2 - Metabolism of dietary glycans is pivotal in shaping the human gut microbiota. However, the mechanisms that promote competition for glycans among gut commensals remain unclear. Roseburia intestinalis, an abundant butyrate-producing Firmicute, is a key degrader of the major dietary fibre xylan. Despite the association of this taxon to a healthy microbiota, insight is lacking into its glycan utilization machinery. Here, we investigate the apparatus that confers R. intestinalis growth on different xylans. R. intestinalis displays a large cell-attached modular xylanase that promotes multivalent and dynamic association to xylan via four xylan-binding modules. This xylanase operates in concert with an ATP-binding cassette transporter to mediate breakdown and selective internalization of xylan fragments. The transport protein of R. intestinalis prefers oligomers of 4-5 xylosyl units, whereas the counterpart from a model xylan-degrading Bacteroides commensal targets larger ligands. Although R. intestinalis and the Bacteroides competitor co-grew in a mixed culture on xylan, R. intestinalis dominated on the preferred transport substrate xylotetraose. These findings highlight the differentiation of capture and transport preferences as a possible strategy to facilitate co-growth on abundant dietary fibres and may offer a unique route to manipulate the microbiota based on glycan transport preferences in therapeutic interventions to boost distinct taxa.

AB - Metabolism of dietary glycans is pivotal in shaping the human gut microbiota. However, the mechanisms that promote competition for glycans among gut commensals remain unclear. Roseburia intestinalis, an abundant butyrate-producing Firmicute, is a key degrader of the major dietary fibre xylan. Despite the association of this taxon to a healthy microbiota, insight is lacking into its glycan utilization machinery. Here, we investigate the apparatus that confers R. intestinalis growth on different xylans. R. intestinalis displays a large cell-attached modular xylanase that promotes multivalent and dynamic association to xylan via four xylan-binding modules. This xylanase operates in concert with an ATP-binding cassette transporter to mediate breakdown and selective internalization of xylan fragments. The transport protein of R. intestinalis prefers oligomers of 4-5 xylosyl units, whereas the counterpart from a model xylan-degrading Bacteroides commensal targets larger ligands. Although R. intestinalis and the Bacteroides competitor co-grew in a mixed culture on xylan, R. intestinalis dominated on the preferred transport substrate xylotetraose. These findings highlight the differentiation of capture and transport preferences as a possible strategy to facilitate co-growth on abundant dietary fibres and may offer a unique route to manipulate the microbiota based on glycan transport preferences in therapeutic interventions to boost distinct taxa.

U2 - 10.1038/s41564-018-0132-8

DO - 10.1038/s41564-018-0132-8

M3 - Journal article

JO - Nature Microbiology

JF - Nature Microbiology

SN - 2058-5276

ER -