Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteria

The colonic mucus layer, comprised of highly O-glycosylated mucins, is vital to mediating host-gut microbiota interactions, yet the impact of dietary changes on colonic mucin O-glycosylation and its associations with the gut microbiota remains unexplored. Here, we used an array of omics techniques i...

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Main Authors: Hasinika K. A. H. Gamage, Raymond W. W. Chong, Daniel Bucio-Noble, Liisa Kautto, Anandwardhan A. Hardikar, Malcolm S. Ball, Mark P. Molloy, Nicolle H. Packer, Ian T. Paulsen
Format: Article
Language:English
Published: Taylor & Francis Group 2020-11-01
Series:Gut Microbes
Subjects:
Online Access:http://dx.doi.org/10.1080/19490976.2020.1802209
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spelling doaj-91edbbf58e2f4d558cb701e845f7f4282021-03-18T15:12:50ZengTaylor & Francis GroupGut Microbes1949-09761949-09842020-11-0112110.1080/19490976.2020.18022091802209Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteriaHasinika K. A. H. Gamage0Raymond W. W. Chong1Daniel Bucio-Noble2Liisa Kautto3Anandwardhan A. Hardikar4Malcolm S. Ball5Mark P. Molloy6Nicolle H. Packer7Ian T. Paulsen8Macquarie UniversityMacquarie UniversityMacquarie UniversityMacquarie UniversityThe University of SydneyGratuk Technologies Pty LtdMacquarie UniversityMacquarie UniversityMacquarie UniversityThe colonic mucus layer, comprised of highly O-glycosylated mucins, is vital to mediating host-gut microbiota interactions, yet the impact of dietary changes on colonic mucin O-glycosylation and its associations with the gut microbiota remains unexplored. Here, we used an array of omics techniques including glycomics to examine the effect of dietary fiber consumption on the gut microbiota, colonic mucin O-glycosylation and host physiology of high-fat diet-fed C57BL/6J mice. The high-fat diet group had significantly impaired glucose tolerance and altered liver proteome, gut microbiota composition, and short-chain fatty acid production compared to normal chow diet group. While dietary fiber inclusion did not reverse all high fat-induced modifications, it resulted in specific changes, including an increase in the relative abundance of bacterial families with known fiber digesters and a higher propionate concentration. Conversely, colonic mucin O-glycosylation remained similar between the normal chow and high-fat diet groups, while dietary fiber intervention resulted in major alterations in O-glycosylation. Correlation network analysis revealed previously undescribed associations between specific bacteria and mucin glycan structures. For example, the relative abundance of the bacterium Parabacteroides distasonis positively correlated with glycan structures containing one terminal fucose and correlated negatively with glycans containing two terminal fucose residues or with both an N-acetylneuraminic acid and a sulfate residue. This is the first comprehensive report of the impact of dietary fiber on the colonic mucin O-glycosylation and associations of these mucosal glycans with specific gut bacteria.http://dx.doi.org/10.1080/19490976.2020.1802209gut microbiotamucin o-glycosylationglycan-microbiota interactiondietary interventiondietary fiber
collection DOAJ
language English
format Article
sources DOAJ
author Hasinika K. A. H. Gamage
Raymond W. W. Chong
Daniel Bucio-Noble
Liisa Kautto
Anandwardhan A. Hardikar
Malcolm S. Ball
Mark P. Molloy
Nicolle H. Packer
Ian T. Paulsen
spellingShingle Hasinika K. A. H. Gamage
Raymond W. W. Chong
Daniel Bucio-Noble
Liisa Kautto
Anandwardhan A. Hardikar
Malcolm S. Ball
Mark P. Molloy
Nicolle H. Packer
Ian T. Paulsen
Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteria
Gut Microbes
gut microbiota
mucin o-glycosylation
glycan-microbiota interaction
dietary intervention
dietary fiber
author_facet Hasinika K. A. H. Gamage
Raymond W. W. Chong
Daniel Bucio-Noble
Liisa Kautto
Anandwardhan A. Hardikar
Malcolm S. Ball
Mark P. Molloy
Nicolle H. Packer
Ian T. Paulsen
author_sort Hasinika K. A. H. Gamage
title Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteria
title_short Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteria
title_full Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteria
title_fullStr Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteria
title_full_unstemmed Changes in dietary fiber intake in mice reveal associations between colonic mucin O-glycosylation and specific gut bacteria
title_sort changes in dietary fiber intake in mice reveal associations between colonic mucin o-glycosylation and specific gut bacteria
publisher Taylor & Francis Group
series Gut Microbes
issn 1949-0976
1949-0984
publishDate 2020-11-01
description The colonic mucus layer, comprised of highly O-glycosylated mucins, is vital to mediating host-gut microbiota interactions, yet the impact of dietary changes on colonic mucin O-glycosylation and its associations with the gut microbiota remains unexplored. Here, we used an array of omics techniques including glycomics to examine the effect of dietary fiber consumption on the gut microbiota, colonic mucin O-glycosylation and host physiology of high-fat diet-fed C57BL/6J mice. The high-fat diet group had significantly impaired glucose tolerance and altered liver proteome, gut microbiota composition, and short-chain fatty acid production compared to normal chow diet group. While dietary fiber inclusion did not reverse all high fat-induced modifications, it resulted in specific changes, including an increase in the relative abundance of bacterial families with known fiber digesters and a higher propionate concentration. Conversely, colonic mucin O-glycosylation remained similar between the normal chow and high-fat diet groups, while dietary fiber intervention resulted in major alterations in O-glycosylation. Correlation network analysis revealed previously undescribed associations between specific bacteria and mucin glycan structures. For example, the relative abundance of the bacterium Parabacteroides distasonis positively correlated with glycan structures containing one terminal fucose and correlated negatively with glycans containing two terminal fucose residues or with both an N-acetylneuraminic acid and a sulfate residue. This is the first comprehensive report of the impact of dietary fiber on the colonic mucin O-glycosylation and associations of these mucosal glycans with specific gut bacteria.
topic gut microbiota
mucin o-glycosylation
glycan-microbiota interaction
dietary intervention
dietary fiber
url http://dx.doi.org/10.1080/19490976.2020.1802209
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