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Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins

The enteropathogenic bacterium, Campylobacter jejuni, was considered to be non‐saccharolytic, but recently it emerged that l‐fucose plays a central role in C. jejuni virulence. Half of C. jejuni clinical isolates possess an operon for l‐fucose utilisation. In the intestinal tract, l‐fucose is abunda...

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Autores principales: Luijkx, Yvette M.C.A., Bleumink, Nancy M.C., Jiang, Jianbing, Overkleeft, Herman S., Wösten, Marc M.S.M., Strijbis, Karin, Wennekes, Tom
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7685106/
https://www.ncbi.nlm.nih.gov/pubmed/32827216
http://dx.doi.org/10.1111/cmi.13252
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author Luijkx, Yvette M.C.A.
Bleumink, Nancy M.C.
Jiang, Jianbing
Overkleeft, Herman S.
Wösten, Marc M.S.M.
Strijbis, Karin
Wennekes, Tom
author_facet Luijkx, Yvette M.C.A.
Bleumink, Nancy M.C.
Jiang, Jianbing
Overkleeft, Herman S.
Wösten, Marc M.S.M.
Strijbis, Karin
Wennekes, Tom
author_sort Luijkx, Yvette M.C.A.
collection PubMed
description The enteropathogenic bacterium, Campylobacter jejuni, was considered to be non‐saccharolytic, but recently it emerged that l‐fucose plays a central role in C. jejuni virulence. Half of C. jejuni clinical isolates possess an operon for l‐fucose utilisation. In the intestinal tract, l‐fucose is abundantly available in mucin O‐linked glycan structures, but C. jejuni lacks a fucosidase enzyme essential to release the l‐fucose. We set out to determine how C. jejuni can gain access to these intestinal l‐fucosides. Growth of the fuc + C. jejuni strains, 129,108 and NCTC 11168, increased in the presence of l‐fucose while fucose permease knockout strains did not benefit from additional l‐fucose. With fucosidase assays and an activity‐based probe, we confirmed that Bacteriodes fragilis, an abundant member of the intestinal microbiota, secretes active fucosidases. In the presence of mucins, C. jejuni was dependent on B. fragilis fucosidase activity for increased growth. Campylobacter jejuni invaded Caco‐2 intestinal cells that express complex O‐linked glycan structures that contain l‐fucose. In infection experiments, C. jejuni was more invasive in the presence of B. fragilis and this increase is due to fucosidase activity. We conclude that C. jejuni fuc + strains are dependent on exogenous fucosidases for increased growth and invasion.
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spelling pubmed-76851062020-12-03 Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins Luijkx, Yvette M.C.A. Bleumink, Nancy M.C. Jiang, Jianbing Overkleeft, Herman S. Wösten, Marc M.S.M. Strijbis, Karin Wennekes, Tom Cell Microbiol Research Articles The enteropathogenic bacterium, Campylobacter jejuni, was considered to be non‐saccharolytic, but recently it emerged that l‐fucose plays a central role in C. jejuni virulence. Half of C. jejuni clinical isolates possess an operon for l‐fucose utilisation. In the intestinal tract, l‐fucose is abundantly available in mucin O‐linked glycan structures, but C. jejuni lacks a fucosidase enzyme essential to release the l‐fucose. We set out to determine how C. jejuni can gain access to these intestinal l‐fucosides. Growth of the fuc + C. jejuni strains, 129,108 and NCTC 11168, increased in the presence of l‐fucose while fucose permease knockout strains did not benefit from additional l‐fucose. With fucosidase assays and an activity‐based probe, we confirmed that Bacteriodes fragilis, an abundant member of the intestinal microbiota, secretes active fucosidases. In the presence of mucins, C. jejuni was dependent on B. fragilis fucosidase activity for increased growth. Campylobacter jejuni invaded Caco‐2 intestinal cells that express complex O‐linked glycan structures that contain l‐fucose. In infection experiments, C. jejuni was more invasive in the presence of B. fragilis and this increase is due to fucosidase activity. We conclude that C. jejuni fuc + strains are dependent on exogenous fucosidases for increased growth and invasion. John Wiley & Sons, Inc. 2020-09-21 2020-12 /pmc/articles/PMC7685106/ /pubmed/32827216 http://dx.doi.org/10.1111/cmi.13252 Text en © 2020 The Authors. Cellular Microbiology published by John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Luijkx, Yvette M.C.A.
Bleumink, Nancy M.C.
Jiang, Jianbing
Overkleeft, Herman S.
Wösten, Marc M.S.M.
Strijbis, Karin
Wennekes, Tom
Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins
title Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins
title_full Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins
title_fullStr Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins
title_full_unstemmed Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins
title_short Bacteroides fragilis fucosidases facilitate growth and invasion of Campylobacter jejuni in the presence of mucins
title_sort bacteroides fragilis fucosidases facilitate growth and invasion of campylobacter jejuni in the presence of mucins
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7685106/
https://www.ncbi.nlm.nih.gov/pubmed/32827216
http://dx.doi.org/10.1111/cmi.13252
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