Reply to “Syntrophic Propionate Oxidation via Butyrate: a Novel Window of Opportunity under Methanogenic Conditions”

REPLY

In a study that evaluated the oxidation of propionate in anoxic microcosms of rice paddy soil, we proposed that both the methylmalonyl-coenzyme A (CoA) pathway and the six-carbon-intermediate (6-C) pathway (see reference 1 for historical work on the 6-C pathway) were involved in the metabolism of propionate (2). Dolfing (3) calculated the Gibbs free energy for these two pathways and concluded that the 6-C pathway (referred to as the Smithella pathway by Dolfing) is thermodynamically more advantageous than the methylmalonyl-CoA pathway (referred to as the classical propionate degradation pathway by Dolfing). He proposed that the 6-C pathway opens a novel window of opportunity for the oxidation of propionate under methanogenic conditions. Smithella species are known to utilize the 6-C pathway and have been detected in various anoxic environments (4, 5), suggesting that this pathway may be widespread.

Dolfing (3) indicated that the utilization of the 6-C pathway could explain why the oxidation of propionate occurred under conditions that were thermodynamically unfavorable for the methylmalonyl-CoA pathway in anoxic incubations of rice paddy soil (6). This is certainly an excellent explanation for the observations reported. However, the experiments with chemostat cocultures of Syntrophobacter fumaroxidans and Methanospirillum hungatei indicate that propionate oxidation via the methylmalonyl-CoA pathway can occur when the Gibbs free energy is greater than −10 kJ per mol propionate (7), a value much lower than the theoretical minimum energy quantum (−20 kJ per mol) needed for the conservation of energy as determined by the synthesis of ATP (8). Thus, even the syntrophs utilizing the methylmalonyl-CoA pathway have probably evolved unusual mechanisms to surpass the unfavorable thermodynamic conditions. In this regard, both Syntrophobacter fumaroxidans and Pelotomaculum thermopropionicum, the classical syntrophs employing the methylmalonyl-CoA pathway, harbor a rich machinery to use formate instead of H₂ as the electron shuttle for the syntrophic interaction (9, 10). It was known that interspecies formate transfer might sustain a 100-fold-higher conversion of substrate than can interspecies H₂ transfer based on Fick's diffusion law (11). Furthermore, it has been shown that P. thermopropionicum synthesizes flagellum-like filaments and extracellular polymers that might stimulate microbial aggregation and enhance interspecies electron transfer with a methanogenic partner (12, 13). These collective observations and the thermodynamic considerations delineated by Dolfing (3) reinforce the likelihood that propionate-utilizing syntrophs have diverse mechanisms to overcome energetic barriers.