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Microbial production of hydrogen (future ideal fuel and important gas for industries) under anoxic conditions has limited ATP availability and low efficiency. We engineered E. coli K12 to acquire a flavin-based electron bifurcation (FBEB) system, a bioenergetic route typically found in strict anaerobes, which uses NADH to generate low potential reduced ferredoxin and high potential butyryl-CoA. The oxygen-tolerant FBEB-E. coli showed higher H2 and succinate production (2-4 folds), lower cellular reduction potentials, greater accumulation of cellular reductants and various metabolites, including ATP (up to a 7-fold increase). It could better tolerate prolonged and recycled usage of the engineered cell for H2 and succinate production than the native strain. FBEB-E. coli could also use various substrates such as formate, D-glucose and food waste for H2 and succinate production. This is a promising pathway to sustainable H2 and succinate production. This work also demonstrates that E. coli with an extra electron bifurcation system is a robust synthetic biology host.

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