Campylobacter jejuni uses energy taxis and a dehydrogenase enzyme for l-fucose chemotaxis

Abstract

ABSTRACTCampylobacter jejuni is a leading cause of bacterial diarrhea worldwide, and infection in infants is associated with growth stunting in low- and middle-income countries. Approximately half of all C. jejuni isolates are asaccharolytic, while the remainder encode enzymes capable of l-fucose catabolism. Our previous study suggested that breastfed infants originating from sub-Saharan Africa and South Asia were colonized less frequently with l-fucose-metabolizing C. jejuni isolates compared to asaccharolytic strains. We also showed that FucX is an l-fucose dehydrogenase that binds to its NADP+ cofactor even in the absence of l-fucose and that this enzyme is sufficient for l-fucose chemotaxis when introduced into strains lacking the metabolic pathway. This study indicates that FucX may influence l-fucose chemotaxis by increasing cellular NADPH/NADP+ ratios, which subsequently affect the energy taxis components, CetABC that respond to shifting gradients of electron acceptors and donors. Furthermore, C. jejuni CetAB and CetAC can complement Escherichia coli aerotaxis. Our data support a model in which the shift in NADP+ levels, impacted by the FucX dehydrogenase, affects chemotaxis in response to l-fucose. This swimming behavior can be phenocopied with a homologous l-fucose dehydrogenase from Burkholderia multivorans. Taken together, our work provides a possible explanation for why l-fucose-metabolizing C. jejuni isolates swim away from intestinal epithelial cells toward free fucose in the lumen where they are subsequently cleared by breastfed infants.IMPORTANCEIn this study, we identify a separate role for the Campylobacter jejuni l-fucose dehydrogenase in l-fucose chemotaxis and demonstrate that this mechanism is not only limited to C. jejuni but is also present in Burkholderia multivorans. We now hypothesize that l-fucose energy taxis may contribute to the reduction of l-fucose-metabolizing strains of C. jejuni from the gastrointestinal tract of breastfed infants, selecting for isolates with increased colonization potential.

Keywords

• Campylobacter jejuni
• l-fucose
• energy taxis
• chemotaxis