Introduction:
Campylobacter jejuni is a major gastrointestinal pathogen generally acquired via consumption of poorly prepared poultry. N-linked protein glycosylation encoded by the pgl gene cluster targets >80 membrane proteins and is required for both non-symptomatic chicken colonization and full human intestinal epithelial cell virulence. Despite this, the biological functions of N-glycosylation remain unknown.
Methodologies:
Here we examined the effects of pgl gene deletion on the C. jejuni proteome using label-based liquid chromatography / tandem mass spectrometry (LC-MS/MS) and validation using data independent analysis (DIA-SWATH-MS). Targeted metabolomics was used to assess the impact of loss of N-glycosylation on intracellular levels of key respiratory metabolites. Other conventional microbial assays, tube-based chemotactic responses, biofilm formation, cell morphology and susceptibility to temperature and osmotic stress, were performed to establish how protein-level changes translated into macro-level phenotypes critical to cell function and pathogenicity.
Key findings:
We quantified 1359 proteins corresponding to ~84% of the predicted C. jejuni NCTC 11168 genome. Deletion of the pglB oligosaccharyltransferase (ΔpglB) resulted in a significant change in abundance of 185 proteins, 137 of which were restored to their wild-type levels by reintroduction of pglB (ΔpglB::ΔpglB). Deletion of pglB was associated with significantly reduced abundances of known pgl targets and increased levels of stress-related proteins. Commensurately, pglB mutants demonstrated reduced survival following temperature (4°C and 46°C) and osmotic (150 mM NaCl) shock, and showed altered biofilm phenotypes compared to wild-type C. jejuni. Targeted metabolomics established that glycosylation negative C. jejuni were depleted of all respiration-associated proteins that allow the use of alternative electron acceptors under low oxygen conditions, which correlated with protein-level changes to known small-molecule transporters. These data indicate a multi-factorial role for N-glycosylation in C. jejuni physiology.