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Discovery of intramolecular trans-sialidases in human gut microbiota suggests novel mechanisms of mucosal adaptation

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Owen_2015_NatComm_Discovery_CC.pdf (1.110Mb)
Date
08/07/2015
Author
Tailford, Louise E.
Owen, C. David
Walshaw, John
Crost, Emmanuelle H.
Hardy-Goddard, Jemma
Le Gall, Gwenaelle
de Vos, Willem M.
Taylor, Garry L.
Juge, Nathalie
Keywords
Inflammatory bowel-diseases
Sialic-acid
Streptococcus-pneumoniae
Entric pathogens
Crystal-structure
Mucus layers
Mucin
Bacteria
Specificity
Metabolism
R Medicine
BDC
R2C
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Abstract
The gastrointestinal mucus layer is colonized by a dense community of microbes catabolizing dietary and host carbohydrates during their expansion in the gut. Alterations in mucosal carbohydrate availability impact on the composition of microbial species. Ruminococcus gnavus is a commensal anaerobe present in the gastrointestinal tract of >90% of humans and overrepresented in inflammatory bowel diseases (IBD). Using a combination of genomics, enzymology and crystallography, we show that the mucin-degrader R. gnavus ATCC 29149 strain produces an intramolecular trans-sialidase (IT-sialidase) that cleaves off terminal α2-3-linked sialic acid from glycoproteins, releasing 2,7-anhydro-Neu5Ac instead of sialic acid. Evidence of IT-sialidases in human metagenomes indicates that this enzyme occurs in healthy subjects but is more prevalent in IBD metagenomes. Our results uncover a previously unrecognized enzymatic activity in the gut microbiota, which may contribute to the adaptation of intestinal bacteria to the mucosal environment in health and disease.
Citation
Tailford , L E , Owen , C D , Walshaw , J , Crost , E H , Hardy-Goddard , J , Le Gall , G , de Vos , W M , Taylor , G L & Juge , N 2015 , ' Discovery of intramolecular trans- sialidases in human gut microbiota suggests novel mechanisms of mucosal adaptation ' , Nature Communications , vol. 6 , 7624 . https://doi.org/10.1038/ncomms8624
Publication
Nature Communications
Status
Peer reviewed
DOI
https://doi.org/10.1038/ncomms8624
ISSN
2041-1723
Type
Journal article
Rights
Copyright 2015 the Authors. This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
Description
The authors acknowledge the support of the Biotechnology and Biological Sciences Research Council (BBSRC), this research was partly funded by the BBSRC Institute Strategic Programme for The Gut Health and Food Safety (BB/J004529/1) and by the BB/L008602/1 BBSRC-responsive mode grant. We also acknowledge support from the EU FP7 TORNADO programme. The research of WMdV was supported by the Academy of Finland, European Research Council and the Netherlands Organization for Scientific Research.
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  • University of St Andrews Research
URI
http://hdl.handle.net/10023/7310

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