Anaerobic microbial metabolism can proceed close to thermodynamic limits

Many fermentative bacteria obtain energy for growth by reactions in which the change in free energy (ΔG′) is less than that needed to synthesize ATP1,2,3,4. These bacteria couple substrate metabolism directly to ATP synthesis, however, by classical phosphoryl transfer reactions4,5. An explanation for the energy economy of these organisms is that biological systems conserve energy in discrete amounts3,4, with a minimum, biochemically convertible energy value of about -20 kJ mol-1 (refs 1, 2, 3). This concept predicts that anaerobic substrate decay ceases before the minimum free energy value is reached, and several studies support this prediction1,6,7,8,9. Here we show that metabolism by syntrophic associations, in which the degradation of a substrate by one species is thermodynamically possible only through removal of the end product by another species1, can occur at values close to thermodynamic equilibrium (ΔG′ ≈ 0 kJ mol-1). The free energy remaining when substrate metabolism halts is not constant; it depends on the terminal electron-accepting reaction and the amount of energy required for substrate activation. Syntrophic associations metabolize near thermodynamic equilibrium, indicating that bacteria operate extremely efficient catabolic systems.