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

Jolene M Garber,Alisdair B Boraston,Christine M Szymanski,Martin Stahl,Ben Pluvinage,Alain Stintzi,Harald Nothaft,Hua Huang,John A Gerlt,Amber Enriquez,Sara Porfirio,Parastoo Azadi,Xiaoming Bian,Eric Line,James Butcher,John Glushka

doi:10.1038/s42003-019-0727-5

Abstract

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.

Highlights

The gastrointestinal pathogen Campylobacter jejuni was considered asaccharolytic, >50% of sequenced isolates possess an operon for L-fucose utilization
Co-culture growth experiments were conducted to determine whether porcine mucin enhances C. jejuni growth in the presence of B. vulgatus and that was what was observed
Fucose metabolism contributed in part to this phenotype since a C. jejuni fucose permease encoded by cj0486 (fucP) mutant showed less growth enhancement under these conditions (Fig. 1b)

Summary

Introduction

The gastrointestinal pathogen Campylobacter jejuni was considered asaccharolytic, >50% of sequenced isolates possess an operon for L-fucose utilization. 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. C. jejuni was once considered asaccharolytic since it lacks key enzymes from the Entner-Doudoroff and pentose phosphate pathways for carbohydrate metabolism. Tricarboxylic acid cycle intermediates and short chain fatty acids regularly found in the gut as by-products of microbial metabolism are used by C. jejuni[4,5] and their spatial distribution may be important for niche establishment in both commensal and pathogenic systems[6].

Methods

Results

Conclusion