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The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus

Although the gastrointestinal pathogen Campylobacter jejuni was considered asaccharolytic, >50% of sequenced isolates possess an operon for l-fucose utilization. In C. jejuni NCTC11168, this pathway confers l-fucose chemotaxis and competitive colonization advantages in the piglet diarrhea model,...

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Autores principales: Garber, Jolene M., Nothaft, Harald, Pluvinage, Ben, Stahl, Martin, Bian, Xiaoming, Porfirio, Sara, Enriquez, Amber, Butcher, James, Huang, Hua, Glushka, John, Line, Eric, Gerlt, John A., Azadi, Parastoo, Stintzi, Alain, Boraston, Alisdair B., Szymanski, Christine M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6946681/
https://www.ncbi.nlm.nih.gov/pubmed/31925306
http://dx.doi.org/10.1038/s42003-019-0727-5
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author Garber, Jolene M.
Nothaft, Harald
Pluvinage, Ben
Stahl, Martin
Bian, Xiaoming
Porfirio, Sara
Enriquez, Amber
Butcher, James
Huang, Hua
Glushka, John
Line, Eric
Gerlt, John A.
Azadi, Parastoo
Stintzi, Alain
Boraston, Alisdair B.
Szymanski, Christine M.
author_facet Garber, Jolene M.
Nothaft, Harald
Pluvinage, Ben
Stahl, Martin
Bian, Xiaoming
Porfirio, Sara
Enriquez, Amber
Butcher, James
Huang, Hua
Glushka, John
Line, Eric
Gerlt, John A.
Azadi, Parastoo
Stintzi, Alain
Boraston, Alisdair B.
Szymanski, Christine M.
author_sort Garber, Jolene M.
collection PubMed
description Although the gastrointestinal pathogen Campylobacter jejuni was considered asaccharolytic, >50% of sequenced isolates possess an operon for l-fucose utilization. In C. jejuni NCTC11168, this pathway confers l-fucose chemotaxis and competitive colonization advantages in the piglet diarrhea model, but the catabolic steps remain unknown. Here we solved the putative dehydrogenase structure, resembling FabG of Burkholderia multivorans. The C. jejuni enzyme, FucX, reduces l-fucose and d-arabinose in vitro and both sugars are catabolized by fuc-operon encoded enzymes. This enzyme alone confers chemotaxis to both sugars in a non-carbohydrate-utilizing C. jejuni strain. Although C. jejuni lacks fucosidases, the organism exhibits enhanced growth in vitro when co-cultured with Bacteroides vulgatus, suggesting scavenging may occur. Yet, when excess amino acids are available, C. jejuni prefers them to carbohydrates, indicating a metabolic hierarchy exists. Overall this study increases understanding of nutrient metabolism by this pathogen, and identifies interactions with other gut microbes.
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spelling pubmed-69466812020-01-13 The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus Garber, Jolene M. Nothaft, Harald Pluvinage, Ben Stahl, Martin Bian, Xiaoming Porfirio, Sara Enriquez, Amber Butcher, James Huang, Hua Glushka, John Line, Eric Gerlt, John A. Azadi, Parastoo Stintzi, Alain Boraston, Alisdair B. Szymanski, Christine M. Commun Biol Article Although the gastrointestinal pathogen Campylobacter jejuni was considered asaccharolytic, >50% of sequenced isolates possess an operon for l-fucose utilization. In C. jejuni NCTC11168, this pathway confers l-fucose chemotaxis and competitive colonization advantages in the piglet diarrhea model, but the catabolic steps remain unknown. Here we solved the putative dehydrogenase structure, resembling FabG of Burkholderia multivorans. The C. jejuni enzyme, FucX, reduces l-fucose and d-arabinose in vitro and both sugars are catabolized by fuc-operon encoded enzymes. This enzyme alone confers chemotaxis to both sugars in a non-carbohydrate-utilizing C. jejuni strain. Although C. jejuni lacks fucosidases, the organism exhibits enhanced growth in vitro when co-cultured with Bacteroides vulgatus, suggesting scavenging may occur. Yet, when excess amino acids are available, C. jejuni prefers them to carbohydrates, indicating a metabolic hierarchy exists. Overall this study increases understanding of nutrient metabolism by this pathogen, and identifies interactions with other gut microbes. Nature Publishing Group UK 2020-01-07 /pmc/articles/PMC6946681/ /pubmed/31925306 http://dx.doi.org/10.1038/s42003-019-0727-5 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Garber, Jolene M.
Nothaft, Harald
Pluvinage, Ben
Stahl, Martin
Bian, Xiaoming
Porfirio, Sara
Enriquez, Amber
Butcher, James
Huang, Hua
Glushka, John
Line, Eric
Gerlt, John A.
Azadi, Parastoo
Stintzi, Alain
Boraston, Alisdair B.
Szymanski, Christine M.
The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus
title The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus
title_full The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus
title_fullStr The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus
title_full_unstemmed The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus
title_short The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus
title_sort gastrointestinal pathogen campylobacter jejuni metabolizes sugars with potential help from commensal bacteroides vulgatus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6946681/
https://www.ncbi.nlm.nih.gov/pubmed/31925306
http://dx.doi.org/10.1038/s42003-019-0727-5
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