The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans

Sabina Leanti La Rosa, Maria Louise Leth, Leszek Michalak, Morten Ejby Hansen, Nicholas A. Pudlo, Robert Glowacki, Gabriel Pereira, Christopher T. Workman, Magnus Arntzen, Phillip B. Pope, Eric C. Martens, Maher Abou Hachem, Bjørge Westereng*

*Corresponding author for this work

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Abstract

β-Mannans are plant cell wall polysaccharides that are commonly found in human diets. However, a mechanistic understanding into the key populations that degrade this glycan is absent, especially for the dominant Firmicutes phylum. Here, we show that the prominent butyrate-producing Firmicute Roseburia intestinalis expresses two loci conferring metabolism of β-mannans. We combine multi-“omic” analyses and detailed biochemical studies to comprehensively characterize loci-encoded proteins that are involved in β-mannan capturing, importation, de-branching and degradation into monosaccharides. In mixed cultures, R. intestinalis shares the available β-mannan with Bacteroides ovatus, demonstrating that the apparatus allows coexistence in a competitive environment. In murine experiments, β-mannan selectively promotes beneficial gut bacteria, exemplified by increased R. intestinalis, and reduction of mucus-degraders. Our findings highlight that R. intestinalis is a primary degrader of this dietary fiber and that this metabolic capacity could be exploited to selectively promote key members of the healthy microbiota using β-mannan-based therapeutic interventions.

Original languageEnglish
Article number905
JournalNature Communications
Volume10
Issue number1
Number of pages14
ISSN2041-1723
DOIs
Publication statusPublished - 2019

Cite this

La Rosa, S. L., Leth, M. L., Michalak, L., Hansen, M. E., Pudlo, N. A., Glowacki, R., ... Westereng, B. (2019). The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans. Nature Communications, 10(1), [905]. https://doi.org/10.1038/s41467-019-08812-y
La Rosa, Sabina Leanti ; Leth, Maria Louise ; Michalak, Leszek ; Hansen, Morten Ejby ; Pudlo, Nicholas A. ; Glowacki, Robert ; Pereira, Gabriel ; Workman, Christopher T. ; Arntzen, Magnus ; Pope, Phillip B. ; Martens, Eric C. ; Hachem, Maher Abou ; Westereng, Bjørge. / The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans. In: Nature Communications. 2019 ; Vol. 10, No. 1.
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abstract = "β-Mannans are plant cell wall polysaccharides that are commonly found in human diets. However, a mechanistic understanding into the key populations that degrade this glycan is absent, especially for the dominant Firmicutes phylum. Here, we show that the prominent butyrate-producing Firmicute Roseburia intestinalis expresses two loci conferring metabolism of β-mannans. We combine multi-“omic” analyses and detailed biochemical studies to comprehensively characterize loci-encoded proteins that are involved in β-mannan capturing, importation, de-branching and degradation into monosaccharides. In mixed cultures, R. intestinalis shares the available β-mannan with Bacteroides ovatus, demonstrating that the apparatus allows coexistence in a competitive environment. In murine experiments, β-mannan selectively promotes beneficial gut bacteria, exemplified by increased R. intestinalis, and reduction of mucus-degraders. Our findings highlight that R. intestinalis is a primary degrader of this dietary fiber and that this metabolic capacity could be exploited to selectively promote key members of the healthy microbiota using β-mannan-based therapeutic interventions.",
author = "{La Rosa}, {Sabina Leanti} and Leth, {Maria Louise} and Leszek Michalak and Hansen, {Morten Ejby} and Pudlo, {Nicholas A.} and Robert Glowacki and Gabriel Pereira and Workman, {Christopher T.} and Magnus Arntzen and Pope, {Phillip B.} and Martens, {Eric C.} and Hachem, {Maher Abou} and Bj{\o}rge Westereng",
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La Rosa, SL, Leth, ML, Michalak, L, Hansen, ME, Pudlo, NA, Glowacki, R, Pereira, G, Workman, CT, Arntzen, M, Pope, PB, Martens, EC, Hachem, MA & Westereng, B 2019, 'The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans', Nature Communications, vol. 10, no. 1, 905. https://doi.org/10.1038/s41467-019-08812-y

The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans. / La Rosa, Sabina Leanti; Leth, Maria Louise; Michalak, Leszek; Hansen, Morten Ejby; Pudlo, Nicholas A.; Glowacki, Robert; Pereira, Gabriel; Workman, Christopher T.; Arntzen, Magnus; Pope, Phillip B.; Martens, Eric C.; Hachem, Maher Abou; Westereng, Bjørge.

In: Nature Communications, Vol. 10, No. 1, 905, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

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T1 - The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans

AU - La Rosa, Sabina Leanti

AU - Leth, Maria Louise

AU - Michalak, Leszek

AU - Hansen, Morten Ejby

AU - Pudlo, Nicholas A.

AU - Glowacki, Robert

AU - Pereira, Gabriel

AU - Workman, Christopher T.

AU - Arntzen, Magnus

AU - Pope, Phillip B.

AU - Martens, Eric C.

AU - Hachem, Maher Abou

AU - Westereng, Bjørge

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N2 - β-Mannans are plant cell wall polysaccharides that are commonly found in human diets. However, a mechanistic understanding into the key populations that degrade this glycan is absent, especially for the dominant Firmicutes phylum. Here, we show that the prominent butyrate-producing Firmicute Roseburia intestinalis expresses two loci conferring metabolism of β-mannans. We combine multi-“omic” analyses and detailed biochemical studies to comprehensively characterize loci-encoded proteins that are involved in β-mannan capturing, importation, de-branching and degradation into monosaccharides. In mixed cultures, R. intestinalis shares the available β-mannan with Bacteroides ovatus, demonstrating that the apparatus allows coexistence in a competitive environment. In murine experiments, β-mannan selectively promotes beneficial gut bacteria, exemplified by increased R. intestinalis, and reduction of mucus-degraders. Our findings highlight that R. intestinalis is a primary degrader of this dietary fiber and that this metabolic capacity could be exploited to selectively promote key members of the healthy microbiota using β-mannan-based therapeutic interventions.

AB - β-Mannans are plant cell wall polysaccharides that are commonly found in human diets. However, a mechanistic understanding into the key populations that degrade this glycan is absent, especially for the dominant Firmicutes phylum. Here, we show that the prominent butyrate-producing Firmicute Roseburia intestinalis expresses two loci conferring metabolism of β-mannans. We combine multi-“omic” analyses and detailed biochemical studies to comprehensively characterize loci-encoded proteins that are involved in β-mannan capturing, importation, de-branching and degradation into monosaccharides. In mixed cultures, R. intestinalis shares the available β-mannan with Bacteroides ovatus, demonstrating that the apparatus allows coexistence in a competitive environment. In murine experiments, β-mannan selectively promotes beneficial gut bacteria, exemplified by increased R. intestinalis, and reduction of mucus-degraders. Our findings highlight that R. intestinalis is a primary degrader of this dietary fiber and that this metabolic capacity could be exploited to selectively promote key members of the healthy microbiota using β-mannan-based therapeutic interventions.

U2 - 10.1038/s41467-019-08812-y

DO - 10.1038/s41467-019-08812-y

M3 - Journal article

VL - 10

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

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ER -