Propionate oxidation by <i>Geobacter sulfurreducens</i> is electron acceptor dependent

ABSTRACT The accumulation of propionate is a challenge in numerous fermentative industrial processes because its degradation is energetically unfavorable and limited to few microbial species. Here, we report for the first time the oxidation of propionate by the extracellular electron transfer (EET)-capable bacterium Geobacter sulfurreducens in axenic cultures. G. sulfurreducens was capable of utilizing propionate both as an electron donor (ED) and a source of carbon, with fumarate as an electron acceptor (EA). In contrast, propionate was metabolized only in the presence of acetate with soluble Fe(III) citrate and was not oxidized when insoluble iron oxides or glassy carbon electrodes poised at +0.1 V vs SHE served as the EA. Biomass yield (per mole of electrons available) was lower with propionate alone than with propionate and acetate together, and acetate was preferentially consumed when both were present. Transcriptomic analysis of cultures grown with either propionate or acetate (with fumarate as EA) showed significant gene expression shifts, strongly suggesting the methylmalonyl-CoA pathway as the main route for propionate degradation. Furthermore, propionate-consuming cultures exhibited an upregulation of branched-chain amino acid (BCAA) biosynthesis, as well as sulfur, nitrogen, and 2-oxocarboxylic acid metabolism. IMPORTANCE The accumulation of propionate is a challenge in anaerobic and fermentative processes because it inhibits methanogenesis, and few microbial species within such systems can degrade it. G. sulfurreducens is a model electroactive bacterium widely used in bioelectrochemical systems and is increasingly studied in wastewater treatment and anaerobic digestion because of its ability to enhance syntrophic metabolism via direct interspecies electron transfer. We show for the first time that G. sulfurreducens can oxidize propionate, expanding its known metabolic repertoire, and that this capability is controlled by the nature of the terminal electron acceptor. Transcriptomic analyses strongly suggest that the methylmalonyl-CoA pathway is the main pathway for propionate degradation and reveal additional associated transcriptional changes. These findings, together with insights into propionate degradation kinetics, could inform future strategies aimed at using this bacterium to mitigate propionate buildup and improve the stability of anaerobic treatment systems.