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‐ (△Go’ = ‐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.

Formation of a functionally active sodium‐translocating hybrid F1F0 ATPase in Escherichia coli by homologous recombination

“…The strictly anaerobic bacterium P. modesturn synthesises ATP by decarboxylationlphosphorylation (Hilpert et al, 1984), which includes the dpNa+-generating methylmalonyl-CoA decarboxylase and the Na+-translocating F,F, ATPase . The two ATPases albeit both members of the F,F, family, are clearly distinct with respect to coupling ion specificity and with respect to sequence similarity which is only weak for most (except a and subunits) of the corresponding subunits (Kaim et al, 1992).…”

“…The small free energy of this reaction (AGO' = -20.6 kJ/mol) is utilized by a membrane-bound methylmalonyl-CoA decarboxylase to establish an electrochemical gradient of Na' (Hilpert et al, 1984;Dimroth, 1987). This Na' gradient is used for ATP synthesis by a Na+-translocating F,Fo ATPase .…”

Methanogenic degradation of acetone by an enrichment culture

“…Since not the whole equivalent of one ATP as with many biotin-dependent carboxylation reactions (Stryer 1981) can be spent in this step, one has to think of a possible membrane-bound mechanism which couples the carboxylation reaction with an ion transport across the membrane, Such a process which requires only fractions of an ATP have been studied in the recent past (Dimroth 1982;Hilpert et al 1984) and a similar mechanism was assumed to operate in methanogenic isovalerate degradation (Stieb and Schink 1986). Our further studies will concentrate on isolating the acetone-fermenting eubacterium and elucidate the pathway of its energy metabolism.…”

Construction, expression and characterization of a plasmid‐encoded Na+‐specific ATPase hybrid consisting of Propionigenium modestum F0‐ATPase and Escherichia coli F1‐ATPase

“…The small free energy of the decarboxylation reaction (AGO' = -20.6 kJ . mol) is exploited by a membrane-bound methylmalonyl-CoA decarboxylase to set up an electrochemical gradient of Na' (Hilpert et al, 1984;. Consequently, ATP synthesis in P. modestum is performed by a Na+-translocating FIFO-ATPase taking advantage of the established Na' gradient Dimroth, 1987, 1988).…”