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 H2 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 H2 partial pressure was measured during the same period. Values of k decreased with increasing H2 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 H2 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 H2 by methanogenic bacteria consuming H2. Gibbs free energies for H2 formation from propionate correlated negatively with the ΔG values for H2 conversion to CH4, but the latter values were generally <−5 kJ mol−1 H2 so that methanogenesis from H2 was always possible. Addition of sulfate did not result in a significant decrease of the ΔG values for H2 formation from propionate demonstrating that H2 consumption by sulfate reducers was not relevant during the short incubation period. Nevertheless, propionate degradation was less strongly inhibited by H2 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 14CO2 and 14CH4) showing that the sulfate reducers oxidized propionate primarily to acetate, bicarbonate and H2. 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 H2‐producing syntrophs.

How specific is the inhibition by methyl fluoride of acetoclastic methanogenesis in anoxic rice field soil?

“…However, relatively small negative vG values are not unusual for propionate degradation in methanogenic paddy soil [24,25]. Again, however, one may argue that thermodynamic conditions in microsites may be even less favorable and that there, acetate and H 2 concentrations are too high to allow the degradation of propionate which then accumulates [21,26].…”

Use of 16S rRNA-targeted oligonucleotide probes to investigate the distribution of sulphate-reducing bacteria in estuarine sediments

“…Moreover, signal from p660 (`Desulfobulbus') has been detected in sediments from a salt marsh [13], an estuary in the UK [5] and a freshwater lake where`Desulfobulbus' was apparently the dominant SRB [6]. Propionate degradation in low-sulphate rice paddy ¢elds appears to be partly mediated by SRB [22,23] and Desulfobulbus-like organisms have been detected in low-sulphate microbial mats [7,24]. These results suggest that Desulfobulbus is involved in the anaerobic degradation of organic matter in both high-and lowsulphate environments.…”

Syntrophobacteraceae‐affiliated species are major propionate‐degrading sulfate reducers in paddy soil

“…Indeed, Syntrophobacter species seem to be key players during methanogenic propionate oxidation in anoxic paddy soil as shown by DNA and RNA-based stable isotope probing analyses (Lueders et al, 2004;Gan et al, 2012). Circumstantial evidence showed that propionate degraders of unknown taxonomic affiliations operated either as SRB or as H 2 producing syntrophs depending on the availability of sulfate in paddy soil (Krylova et al, 1997;Krylova and Conrad, 1998), methanogenic digestors (Wu et al, 1991;Zellner and Neud€ orfer, 1995) and lake sediments (Conrad et al, 1987). Comparisons of the dsrAB diversity in soils from various geographic locations revealed that Syntrophobacter related microorganisms are widespread in low-sulfate peatlands (Steger et al, 2011).…”