Syntrophic butyrate and propionate oxidation processes: from genomes to reaction mechanisms

Abstract

In anoxic environments such as swamps, rice fields and sludge digestors, syntrophic microbial communities are important for decomposition of organic matter to CO2 and CH4 . The most difficult step is the fermentative degradation of short-chain fatty acids such as propionate and butyrate. Conversion of these metabolites to acetate, CO2 , formate and hydrogen is endergonic under standard conditions and occurs only if methanogens keep the concentrations of these intermediate products low. Butyrate and propionate degradation pathways include oxidation steps of comparably high redox potential, i.e. oxidation of butyryl-CoA to crotonyl-CoA and of succinate to fumarate, respectively, that require investment of energy to release the electrons as hydrogen or formate. Although investigated for several decades, the biochemistry of these reactions is still not completely understood. Genome analysis of the butyrate-oxidizing Syntrophomonas wolfei and Syntrophus aciditrophicus and of the propionate-oxidizing Syntrophobacter fumaroxidans and Pelotomaculum thermopropionicum reveals the presence of energy-transforming protein complexes. Recent studies indicated that S. wolfei uses electron-transferring flavoproteins coupled to a menaquinone loop to drive butyryl-CoA oxidation, and that S. fumaroxidans uses a periplasmic formate dehydrogenase, cytochrome b:quinone oxidoreductases, a menaquinone loop and a cytoplasmic fumarate reductase to drive energy-dependent succinate oxidation. Furthermore, we propose that homologues of the Thermotoga maritima bifurcating [FeFe]-hydrogenase are involved in NADH oxidation by S. wolfei and S. fumaroxidans to form hydrogen.

Straw- and slurry-associated prokaryotic communities differ during co-fermentation of straw and swine manure

“…Transformation of propionate into acetate and H 2 can only be realized via syntrophic metabolism under methanogenic condition (Stams and Plugge 2009). Some pure cultures including genera Pelotomaculum, Syntrophobacter, Smithella, and Desulfotomaculum are the hitherto identified propionate oxidizers (Muller et al 2010). In this study, a positive (p<0.05) corre lation between gen us Peloto maculum and Methanoculleus further suggested that the Pelotomaculum was likely to be involved in H 2 and acetate production.…”

Trace element requirements for stable food waste digestion at elevated ammonia concentrations

“…The experimental results do not, however, conclusively prove this original hypothesis as the oxidation of propionic acid, with its uneven carbon chain length, produces a mixed product of acetate, CO 2 , H 2 and formate (Mueller et al, 2010), with side-reactions to produce butyrate and higher-chain fatty acids (de Bok et al, 2001;Stams et al, 1998). The enzymes required for propionic acid oxidation may themselves require the trace elements Se, Mo, and W (de Bok et al, 2003;Mueller et al, 2010;Worm et al, 2011). It has long been recognised, however, that the syntrophic degradation of propionate can be inhibited by a product-induced feedback inhibition (Dong, 1994;Fukuzaki et al, 1990;Kus and Wiesmann, 1995).…”

Tungsten and Molybdenum Regulation of Formate Dehydrogenase Expression in Desulfovibrio vulgaris Hildenborough

“…In Methanococcus vannielii, a single FDH was reported when cells were grown in the presence of tungsten, whereas two enzymes were observed in its absence (22). In Syntrophobacter fumaroxidans, a syntrophic acetogenic bacterium that can also grow by reduction of sulfate or fumarate, two W-containing FDHs have been isolated (12), and several others are encoded in the genome (32). In this organism, growth in the presence of W also leads to a strong increase in total FDH activity relative to growth with Mo, either during syntrophic growth with a methanogen or during growth with propionate and fumarate (35).…”