It has long been thought that Clostridium and its relatives couple the oxidation of one substrate to the reduction of another, yielding energy in the former step and re-achieving redox balance with the latter. By probing the genetics of reductive metabolic pathways in the gut resident C. sporogenes, we find unexpectedly that electron transfer complexes are required for the production of reduced metabolites. Physiologic measurements in vitro indicate that the reductive pathways are coupled to ATP formation, revealing that energy is captured not just during substrate oxidation, but also during coupled reduction, accounting for ~40% of the ATP generated in the cell. Electron transfer complex mutants are attenuated for growth in the mouse gut, demonstrating the importance of energy capture during reductive metabolism for gut colonization. Our findings revise a long-standing model for energy capture by Clostridium sp., and they reveal that the production of high-abundance molecules by a commensal bacterium within the host gut is linked to an energy yielding redox process.