Life by a new decarboxylation-dependent energy conservation mechanism with Na+ as coupling ion

Abstract

We report here a new mode of ATP synthesis in living cells. The anaerobic bacterium Propionigenium modestum gains its total energy for growth from the conversion of succinate to propionate according to: succinate + H₂O → propionate + HCO₃^‐ (△G^o’ = ‐20.6 kJ/mol). The small free energy change of this reaction does not allow a substrate‐linked phosphorylation mechanism, and no electron transport phosphorylation takes place. Succinate was degraded by cell‐free extracts to propionate and CO₂ via succinyl‐CoA, methyl‐malonyl‐CoA and propionyl‐CoA. This pathway involves a membrane‐bound methylmalonyl‐CoA decarboxylase which couples the exergonic decarboxylation with a Na⁺ ion transport across the membrane. The organism also contained a membrane‐bound ATPase which was specifically activated by Na⁺ ions and catalyzed and transport of Na⁺ ions into inverted bacterial vesicles upon ATP hydrolysis. The transport was abolished by monensin but not by the uncoupler carbonylcyanide‐p‐trifluoromethoxy phenylhydrazone. Isolated membrane vesicles catalyzed the synthesis of ATP from ADP and inorganic phosphate when malonyl‐CoA was decarboxylated and malonyl‐CoA synthesis from acetyl‐CoA when ATP was hydrolyzed. These syntheses were sensitive to monensin which indicates that Na⁺ functions as the coupling ion. We conclude from these results that ATP synthesis in P. modestum is driven by a Na⁺ ion gradient which is generated upon decarboxylation of methylmalonyl‐CoA.