Thermodynamics of propionate degradation in methanogenic paddy soil

Abstract

Propionate is syntrophically degraded in methanogenic paddy soil via a randomizing pathway. To study the thermodynamic conditions of this syntrophy, propionate degradation was measured in the presence of different H 2 partial pressures (1–20 000 Pa) using methanogenic soil slurries taken from planted Italian paddy soil. The logarithmic decrease of [1- 14C]propionate or [2- 14C]propionate was measured during an incubation period of about 2–3 h to determine degradation rate constants ( k). The change of the H 2 partial pressure was measured during the same period. Values of k decreased with increasing H 2 partial pressures (averaged over the incubation period). However, k was still relatively high, although the Gibbs free energy (ΔG) of syntrophic propionate conversion to acetate, bicarbonate and H 2 was already strongly endergonic reaching ΔG values of +60 kJ mol −1 propionate. Assuming propionate conversion to acetate plus formate resulted in the same or even higher ΔG values indicating that this degradation pathway was not realistic. We therefore assume that propionate was degraded within microbial aggregates in which syntrophic propionate degraders were shielded from thermodynamically unfavorable H 2 by methanogenic bacteria consuming H 2. Gibbs free energies for H 2 formation from propionate correlated negatively with the ΔG values for H 2 conversion to CH 4, but the latter values were generally <−5 kJ mol −1 H 2 so that methanogenesis from H 2 was always possible. Addition of sulfate did not result in a significant decrease of the ΔG values for H 2 formation from propionate demonstrating that H 2 consumption by sulfate reducers was not relevant during the short incubation period. Nevertheless, propionate degradation was less strongly inhibited by H 2 when sulfate was present indicating that propionate was then mainly degraded by sulfate reduction rather than by syntrophy. The major degradation product of [2- 14C]propionate was 14C-acetate (followed by 14CO 2 and 14CH 4) showing that the sulfate reducers oxidized propionate primarily to acetate, bicarbonate and H 2. As a conceptual model we therefore speculate that propionate was degraded within methanogenic bacterial aggregates both in the presence and the absence of sulfate and that propionate degraders operated either as sulfate reducers or as H 2-producing syntrophs.