Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity

Abstract

Campylobacter concisus is an emerging enteric pathogen that is associated with inflammatory bowel disease. Previous studies demonstrated that C. concisus is non-saccharolytic and hydrogen gas (H2) is a critical factor for C. concisus growth. In order to understand the molecular basis of the non-saccharolytic and H2-dependent nature of C. concisus growth, in this study we examined the pathways involving energy metabolism and oxidative stress defence in C. concisus. Bioinformatic analysis of C. concisus genomes in comparison with the well-studied enteric pathogen Campylobacter jejuni was performed. This study found that C. concisus lacks a number of key enzymes in glycolysis, including glucokinase and phosphofructokinase, and the oxidative pentose phosphate pathway. C. concisus has an incomplete tricarboxylic acid cycle, with no identifiable succinyl-CoA synthase or fumarate hydratase. C. concisus was inferred to use fewer amino acids and have fewer candidate substrates as electron donors and acceptors compared to C. jejuni. The addition of DMSO or fumarate to media resulted in significantly increased growth of C. concisus in the presence of H2 as an electron donor, demonstrating that both can be used as electron acceptors. Catalase, an essential enzyme for oxidative stress defence in C. jejuni, and various nitrosative stress enzymes, were not found in the C. concisus genome. Overall, C. concisus is inferred to have a non-saccharolytic metabolism in which H2 is central to energy conservation, and a narrow selection of carboxylic acids and amino acids can be utilised as organic substrates. In conclusion, this study provides a molecular basis for the non-saccharolytic and hydrogen-dependent nature of C. concisus energy metabolism pathways, which provides insights into the growth requirements and pathogenicity of this species.