The outer mucus layer hosts a distinct intestinal microbial niche

Hai Li; Julien P. Limenitakis; Tobias Fuhrer; Markus B. Geuking; Melissa A. Lawson; Madeleine Wyss; Sandrine Brugiroux; Irene Keller; James MacPherson; Sandra Rupp; Bettina Stolp; Jens V. Stein; Bärbel Stecher; Uwe Sauer; Kathy D. McCoy; Andrew J. Macpherson

doi:10.1038/ncomms9292

The outer mucus layer hosts a distinct intestinal microbial niche

Hai Li, Julien P. Limenitakis, Tobias Fuhrer, Markus B. Geuking, Melissa A. Lawson, Madeleine Wyss, Sandrine Brugiroux, Irene Keller, James MacPherson, Sandra Rupp, Bettina Stolp, Jens V. Stein, Bärbel Stecher, Uwe Sauer, Kathy D. McCoy, Andrew J. Macpherson^*

^*Corresponding author for this work

Randall Centre of Cell & Molecular Biophysics

Research output: Contribution to journal › Article › peer-review

373 Citations (Scopus)

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Abstract

The overall composition of the mammalian intestinal microbiota varies between individuals: within each individual there are differences along the length of the intestinal tract related to host nutrition, intestinal motility and secretions. Mucus is a highly regenerative protective lubricant glycoprotein sheet secreted by host intestinal goblet cells; the inner mucus layer is nearly sterile. Here we show that the outer mucus of the large intestine forms a unique microbial niche with distinct communities, including bacteria without specialized mucolytic capability. Bacterial species present in the mucus show differential proliferation and resource utilization compared with the same species in the intestinal lumen, with high recovery of bioavailable iron and consumption of epithelial-derived carbon sources according to their genome-encoded metabolic repertoire. Functional competition for existence in this intimate layer is likely to be a major determinant of microbiota composition and microbial molecular exchange with the host.

Original language	English
Article number	8292
Journal	Nature Communications
Volume	6
DOIs	https://doi.org/10.1038/ncomms9292
Publication status	Published - 22 Sept 2015

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title = "The outer mucus layer hosts a distinct intestinal microbial niche",

abstract = "The overall composition of the mammalian intestinal microbiota varies between individuals: within each individual there are differences along the length of the intestinal tract related to host nutrition, intestinal motility and secretions. Mucus is a highly regenerative protective lubricant glycoprotein sheet secreted by host intestinal goblet cells; the inner mucus layer is nearly sterile. Here we show that the outer mucus of the large intestine forms a unique microbial niche with distinct communities, including bacteria without specialized mucolytic capability. Bacterial species present in the mucus show differential proliferation and resource utilization compared with the same species in the intestinal lumen, with high recovery of bioavailable iron and consumption of epithelial-derived carbon sources according to their genome-encoded metabolic repertoire. Functional competition for existence in this intimate layer is likely to be a major determinant of microbiota composition and microbial molecular exchange with the host.",

author = "Hai Li and Limenitakis, {Julien P.} and Tobias Fuhrer and Geuking, {Markus B.} and Lawson, {Melissa A.} and Madeleine Wyss and Sandrine Brugiroux and Irene Keller and James MacPherson and Sandra Rupp and Bettina Stolp and Stein, {Jens V.} and B{\"a}rbel Stecher and Uwe Sauer and McCoy, {Kathy D.} and Macpherson, {Andrew J.}",

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AU - Li, Hai

AU - Limenitakis, Julien P.

AU - Fuhrer, Tobias

AU - Geuking, Markus B.

AU - Lawson, Melissa A.

AU - Wyss, Madeleine

AU - Brugiroux, Sandrine

AU - Keller, Irene

AU - MacPherson, James

AU - Rupp, Sandra

AU - Stolp, Bettina

AU - Stein, Jens V.

AU - Stecher, Bärbel

AU - Sauer, Uwe

AU - McCoy, Kathy D.

AU - Macpherson, Andrew J.

PY - 2015/9/22

Y1 - 2015/9/22

N2 - The overall composition of the mammalian intestinal microbiota varies between individuals: within each individual there are differences along the length of the intestinal tract related to host nutrition, intestinal motility and secretions. Mucus is a highly regenerative protective lubricant glycoprotein sheet secreted by host intestinal goblet cells; the inner mucus layer is nearly sterile. Here we show that the outer mucus of the large intestine forms a unique microbial niche with distinct communities, including bacteria without specialized mucolytic capability. Bacterial species present in the mucus show differential proliferation and resource utilization compared with the same species in the intestinal lumen, with high recovery of bioavailable iron and consumption of epithelial-derived carbon sources according to their genome-encoded metabolic repertoire. Functional competition for existence in this intimate layer is likely to be a major determinant of microbiota composition and microbial molecular exchange with the host.

AB - The overall composition of the mammalian intestinal microbiota varies between individuals: within each individual there are differences along the length of the intestinal tract related to host nutrition, intestinal motility and secretions. Mucus is a highly regenerative protective lubricant glycoprotein sheet secreted by host intestinal goblet cells; the inner mucus layer is nearly sterile. Here we show that the outer mucus of the large intestine forms a unique microbial niche with distinct communities, including bacteria without specialized mucolytic capability. Bacterial species present in the mucus show differential proliferation and resource utilization compared with the same species in the intestinal lumen, with high recovery of bioavailable iron and consumption of epithelial-derived carbon sources according to their genome-encoded metabolic repertoire. Functional competition for existence in this intimate layer is likely to be a major determinant of microbiota composition and microbial molecular exchange with the host.

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VL - 6

JO - Nature Communications

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The outer mucus layer hosts a distinct intestinal microbial niche

Abstract

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