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Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization

Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization
Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization

Many intestinal pathogens, including Clostridioides difficile, use mucus-derived sugars as crucial nutrients in the gut. Commensals that compete with pathogens for such nutrients are therefore ecological gatekeepers in healthy guts, and are attractive candidates for therapeutic interventions. Nevertheless, there is a poor understanding of which commensals use mucin-derived sugars in situ as well as their potential to impede pathogen colonization. Here, we identify mouse gut commensals that utilize mucus-derived monosaccharides within complex communities using single-cell stable isotope probing, Raman-activated cell sorting and mini-metagenomics. Sequencing of cell-sorted fractions reveals members of the underexplored family Muribaculaceae as major mucin monosaccharide foragers, followed by members of Lachnospiraceae, Rikenellaceae, and Bacteroidaceae families. Using this information, we assembled a five-member consortium of sialic acid and N-acetylglucosamine utilizers that impedes C. difficile's access to these mucosal sugars and impairs pathogen colonization in antibiotic-treated mice. Our findings underscore the value of targeted approaches to identify organisms utilizing key nutrients and to rationally design effective probiotic mixtures.

Acetylglucosamine/metabolism, Animals, Anti-Bacterial Agents, Bacterial Proteins/metabolism, Bacterial Toxins/metabolism, Cell Separation/methods, Clostridioides difficile/genetics, Clostridium Infections/microbiology, Deuterium, Female, Gastric Mucins/chemistry, Gastrointestinal Microbiome/physiology, Intestinal Mucosa/drug effects, Metagenome, Mice, Inbred C57BL, Monosaccharides/metabolism, N-Acetylneuraminic Acid/metabolism, Polysaccharides/chemistry, Spectrum Analysis, Raman
2041-1723
5104
Pereira, Fátima C
a9396948-26f9-4f13-8f83-a22fec1dd0e0
Wasmund, Kenneth
5e0af83f-4d25-479d-bde2-a55863d92280
Cobankovic, Iva
6978582a-eeb2-40e1-828a-730286cd3f06
Jehmlich, Nico
05633e62-4414-47ba-b230-5d44a9f94bda
Herbold, Craig W
5766a3c8-2906-48d9-9a77-de466a928918
Lee, Kang Soo
4299fa32-f72b-42ce-acba-a116564a36f5
Sziranyi, Barbara
b5fb14d8-dfcc-4a5e-b268-1e8fb0f91e04
Vesely, Cornelia
3ba3d31b-3b6b-42b6-8d92-e82efdd90bdc
Decker, Thomas
79bf2f70-bac3-4029-8e7d-98579e0da072
Stocker, Roman
1a16d8b3-826d-4959-89fa-6c66c60307c2
Warth, Benedikt
8bfd5c28-1a93-484b-8af7-cab4a009503c
von Bergen, Martin
95349f90-50c5-485d-8d66-c6b383a91f5e
Wagner, Michael
b1db4f29-c6dc-444b-b750-5f6a7afcfab7
Berry, David
95147ae5-12bf-4955-af86-dd81c3a1375d
Pereira, Fátima C
a9396948-26f9-4f13-8f83-a22fec1dd0e0
Wasmund, Kenneth
5e0af83f-4d25-479d-bde2-a55863d92280
Cobankovic, Iva
6978582a-eeb2-40e1-828a-730286cd3f06
Jehmlich, Nico
05633e62-4414-47ba-b230-5d44a9f94bda
Herbold, Craig W
5766a3c8-2906-48d9-9a77-de466a928918
Lee, Kang Soo
4299fa32-f72b-42ce-acba-a116564a36f5
Sziranyi, Barbara
b5fb14d8-dfcc-4a5e-b268-1e8fb0f91e04
Vesely, Cornelia
3ba3d31b-3b6b-42b6-8d92-e82efdd90bdc
Decker, Thomas
79bf2f70-bac3-4029-8e7d-98579e0da072
Stocker, Roman
1a16d8b3-826d-4959-89fa-6c66c60307c2
Warth, Benedikt
8bfd5c28-1a93-484b-8af7-cab4a009503c
von Bergen, Martin
95349f90-50c5-485d-8d66-c6b383a91f5e
Wagner, Michael
b1db4f29-c6dc-444b-b750-5f6a7afcfab7
Berry, David
95147ae5-12bf-4955-af86-dd81c3a1375d

Pereira, Fátima C, Wasmund, Kenneth, Cobankovic, Iva, Jehmlich, Nico, Herbold, Craig W, Lee, Kang Soo, Sziranyi, Barbara, Vesely, Cornelia, Decker, Thomas, Stocker, Roman, Warth, Benedikt, von Bergen, Martin, Wagner, Michael and Berry, David (2020) Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization. Nature Communications, 11 (1), 5104, [5104]. (doi:10.1038/s41467-020-18928-1).

Record type: Article

Abstract

Many intestinal pathogens, including Clostridioides difficile, use mucus-derived sugars as crucial nutrients in the gut. Commensals that compete with pathogens for such nutrients are therefore ecological gatekeepers in healthy guts, and are attractive candidates for therapeutic interventions. Nevertheless, there is a poor understanding of which commensals use mucin-derived sugars in situ as well as their potential to impede pathogen colonization. Here, we identify mouse gut commensals that utilize mucus-derived monosaccharides within complex communities using single-cell stable isotope probing, Raman-activated cell sorting and mini-metagenomics. Sequencing of cell-sorted fractions reveals members of the underexplored family Muribaculaceae as major mucin monosaccharide foragers, followed by members of Lachnospiraceae, Rikenellaceae, and Bacteroidaceae families. Using this information, we assembled a five-member consortium of sialic acid and N-acetylglucosamine utilizers that impedes C. difficile's access to these mucosal sugars and impairs pathogen colonization in antibiotic-treated mice. Our findings underscore the value of targeted approaches to identify organisms utilizing key nutrients and to rationally design effective probiotic mixtures.

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More information

Accepted/In Press date: 18 September 2020
Published date: 9 October 2020
Additional Information: Copyright © 2020, The Author(s)
Keywords: Acetylglucosamine/metabolism, Animals, Anti-Bacterial Agents, Bacterial Proteins/metabolism, Bacterial Toxins/metabolism, Cell Separation/methods, Clostridioides difficile/genetics, Clostridium Infections/microbiology, Deuterium, Female, Gastric Mucins/chemistry, Gastrointestinal Microbiome/physiology, Intestinal Mucosa/drug effects, Metagenome, Mice, Inbred C57BL, Monosaccharides/metabolism, N-Acetylneuraminic Acid/metabolism, Polysaccharides/chemistry, Spectrum Analysis, Raman

Identifiers

Local EPrints ID: 470655
URI: http://eprints.soton.ac.uk/id/eprint/470655
ISSN: 2041-1723
PURE UUID: 65384865-c08b-4040-babc-f11d680cf831
ORCID for Fátima C Pereira: ORCID iD orcid.org/0000-0002-1288-6481

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Date deposited: 17 Oct 2022 16:46
Last modified: 17 Mar 2024 04:14

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Contributors

Author: Fátima C Pereira ORCID iD
Author: Kenneth Wasmund
Author: Iva Cobankovic
Author: Nico Jehmlich
Author: Craig W Herbold
Author: Kang Soo Lee
Author: Barbara Sziranyi
Author: Cornelia Vesely
Author: Thomas Decker
Author: Roman Stocker
Author: Benedikt Warth
Author: Martin von Bergen
Author: Michael Wagner
Author: David Berry

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