TY - JOUR
T1 - The gastrointestinal pathogen Campylobacter jejuni metabolizes sugars with potential help from commensal Bacteroides vulgatus
AU - Garber, Jolene M.
AU - Nothaft, Harald
AU - Pluvinage, Ben
AU - Stahl, Martin
AU - Bian, Xiaoming
AU - Porfirio, Sara
AU - Enriquez, Amber
AU - Butcher, James
AU - Huang, Hua
AU - Glushka, John
AU - Line, Eric
AU - Gerlt, John A.
AU - Azadi, Parastoo
AU - Stintzi, Alain
AU - Boraston, Alisdair B.
AU - Szymanski, Christine M.
N1 - Funding Information:
The authors would like to thank David Kelly, Victoria Korolik, Evgeny Vinogradov and Hanwen Huang for helpful discussions. CMS is an Alberta Innovates Strategic Chair in Bacterial Glycomics. This research was supported by Discovery (RGPIN 2014-04355) from the Natural Sciences and Engineering Research Council of Canada to ABB and the National Institutes of Health funded Research Resource for Biomedical Glycomics (P41GM10349010) to PA. Research in the AS laboratory is supported by CIHR grant MOP#84224.
Publisher Copyright:
© 2020, The Author(s).
PY - 2020/12/1
Y1 - 2020/12/1
N2 - 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.
AB - 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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U2 - 10.1038/s42003-019-0727-5
DO - 10.1038/s42003-019-0727-5
M3 - Article
C2 - 31925306
AN - SCOPUS:85077534316
VL - 3
JO - Communications Biology
JF - Communications Biology
SN - 2399-3642
IS - 1
M1 - 2
ER -