Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.

Commensal bacteria often have an especially rich source of glycan-degrading enzymes which allow them to utilize undigested carbohydrates from the food or the host. The species Ruminococcus gnavus is present in the digestive tract of ≥90% of humans and has been implicated in gut-related diseases such...

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Main Authors: Emmanuelle H Crost, Louise E Tailford, Gwenaelle Le Gall, Michel Fons, Bernard Henrissat, Nathalie Juge
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24204617/?tool=EBI
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spelling doaj-f6d894b98b704f8fbf268a3e5a2afe042021-03-04T12:36:01ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-01810e7634110.1371/journal.pone.0076341Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.Emmanuelle H CrostLouise E TailfordGwenaelle Le GallMichel FonsBernard HenrissatNathalie JugeCommensal bacteria often have an especially rich source of glycan-degrading enzymes which allow them to utilize undigested carbohydrates from the food or the host. The species Ruminococcus gnavus is present in the digestive tract of ≥90% of humans and has been implicated in gut-related diseases such as inflammatory bowel diseases (IBD). Here we analysed the ability of two R. gnavus human strains, E1 and ATCC 29149, to utilize host glycans. We showed that although both strains could assimilate mucin monosaccharides, only R. gnavus ATCC 29149 was able to grow on mucin as a sole carbon source. Comparative genomic analysis of the two R. gnavus strains highlighted potential clusters and glycoside hydrolases (GHs) responsible for the breakdown and utilization of mucin-derived glycans. Transcriptomic and functional activity assays confirmed the importance of specific GH33 sialidase, and GH29 and GH95 fucosidases in the mucin utilisation pathway. Notably, we uncovered a novel pathway by which R. gnavus ATCC 29149 utilises sialic acid from sialylated substrates. Our results also demonstrated the ability of R. gnavus ATCC 29149 to produce propanol and propionate as the end products of metabolism when grown on mucin and fucosylated glycans. These new findings provide molecular insights into the strain-specificity of R. gnavus adaptation to the gut environment advancing our understanding of the role of gut commensals in health and disease.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24204617/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Emmanuelle H Crost
Louise E Tailford
Gwenaelle Le Gall
Michel Fons
Bernard Henrissat
Nathalie Juge
spellingShingle Emmanuelle H Crost
Louise E Tailford
Gwenaelle Le Gall
Michel Fons
Bernard Henrissat
Nathalie Juge
Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.
PLoS ONE
author_facet Emmanuelle H Crost
Louise E Tailford
Gwenaelle Le Gall
Michel Fons
Bernard Henrissat
Nathalie Juge
author_sort Emmanuelle H Crost
title Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.
title_short Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.
title_full Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.
title_fullStr Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.
title_full_unstemmed Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent.
title_sort utilisation of mucin glycans by the human gut symbiont ruminococcus gnavus is strain-dependent.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description Commensal bacteria often have an especially rich source of glycan-degrading enzymes which allow them to utilize undigested carbohydrates from the food or the host. The species Ruminococcus gnavus is present in the digestive tract of ≥90% of humans and has been implicated in gut-related diseases such as inflammatory bowel diseases (IBD). Here we analysed the ability of two R. gnavus human strains, E1 and ATCC 29149, to utilize host glycans. We showed that although both strains could assimilate mucin monosaccharides, only R. gnavus ATCC 29149 was able to grow on mucin as a sole carbon source. Comparative genomic analysis of the two R. gnavus strains highlighted potential clusters and glycoside hydrolases (GHs) responsible for the breakdown and utilization of mucin-derived glycans. Transcriptomic and functional activity assays confirmed the importance of specific GH33 sialidase, and GH29 and GH95 fucosidases in the mucin utilisation pathway. Notably, we uncovered a novel pathway by which R. gnavus ATCC 29149 utilises sialic acid from sialylated substrates. Our results also demonstrated the ability of R. gnavus ATCC 29149 to produce propanol and propionate as the end products of metabolism when grown on mucin and fucosylated glycans. These new findings provide molecular insights into the strain-specificity of R. gnavus adaptation to the gut environment advancing our understanding of the role of gut commensals in health and disease.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24204617/?tool=EBI
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