Intestinal inflammation is frequently associated with an alteration of the gut microbiota, termed dysbiosis, which is characterized by a reduced abundance of obligate anaerobic bacteria and an expansion of facultative Proteobacteria such as commensal E. coli. The mechanisms enabling the outgrowth of Proteobacteria during inflammation are incompletely understood. Metagenomic sequencing revealed bacterial formate oxidation and aerobic respiration to be overrepresented metabolic pathways in a chemically induced murine model of colitis. Dysbiosis was accompanied by increased formate levels in the gut lumen. Formate was of microbial origin since no formate was detected in germ-free mice. Complementary studies using commensal E. coli strains as model organisms indicated that formate dehydrogenase and terminal oxidase genes provided a fitness advantage in murine models of colitis. In vivo, formate served as electron donor in conjunction with oxygen as the terminal electron acceptor. This work identifies bacterial formate oxidation and oxygen respiration as metabolic signatures for inflammation-associated dysbiosis. Display omitted •Genes encoding respiratory pathways are overrepresented in the dysbiotic microbiome•Utilization of microbiota-derived formate enhances E. coli fitness in the inflamed gut•Formate concentrations in the gut are elevated during inflammation-associated dysbiosis•During gut inflammation, formate utilization by E. coli requires oxygen respiration Intestinal inflammation is associated with changes in the microbiota composition (dysbiosis), such as the expansion of the commensal Enterobacteriaceae population. Hughes and Winter et al. show that utilization of microbiota-derived formate as electron donor and oxygen as terminal electron acceptor contribute to the bloom of Enterobacteriaceae in the inflamed gut.