Thermophilic archaea activate butane via alkyl-CoM formation

The anaerobic formation and oxidation of methane involve unique enzymatic mechanisms and cofactors, all of which are believed to be specific for C1-compounds. Here we show that an anaerobic thermophilic enrichment culture composed of dense consortia of archaea and bacteria apparently uses partly similar pathways to oxidize the C4 hydrocarbon butane. The archaea, proposed genus ‘Candidatus Syntrophoarchaeum’, show the characteristic autofluorescence of methanogens, and contain highly expressed genes encoding enzymes similar to methyl-coenzyme M reductase. We detect butyl-coenzyme M, indicating archaeal butane activation analogous to the first step in anaerobic methane oxidation. In addition, Ca. Syntrophoarchaeum expresses the genes encoding β-oxidation enzymes, carbon monoxide dehydrogenase and reversible C1 methanogenesis enzymes. This allows for the complete oxidation of butane. Reducing equivalents are seemingly channelled to HotSeep-1, a thermophilic sulfate-reducing partner bacterium known from the anaerobic oxidation of methane. Genes encoding 16S rRNA and methyl-coenzyme M reductase similar to those identifying Ca. Syntrophoarchaeum were repeatedly retrieved from marine subsurface sediments, suggesting that the presented activation mechanism is naturally widespread in the anaerobic oxidation of short-chain hydrocarbons

Methanogens: Syntrophic Metabolism

Syntrophy is a mutualistic interaction in which two metabolically different types of microorganisms are linked by the need to keep metabolites exchanged between the two partners at low concentrations to make the overall metabolism of both organisms feasible. In most cases, the cooperation is based on the transfer of hydrogen, formate, or acetate from fermentative bacteria to methanogens to make the degradation of electron-rich substrates thermodynamically favorable. Syntrophic metabolism proceeds at very low Gibbs’ free energy changes, close to the minimum free energy change needed to conserve energy biologically, which is the energy needed to transport one proton across the cytoplasmic membrane. Pathways for syntrophic degradation of fatty acids predict the net synthesis of about one-third of an ATP per round of catabolism. Syntrophic metabolism entails critical oxidation-reduction reactions in which H2 or formate production would be thermodynamically unfavorable unless energy is invested. Molecular insights into the membrane processes involved in ion translocation and reverse electron transport revealed that syntrophs harbor multiple systems for reverse electron transfer. While much evidence supports the interspecies transfer of H2 and formate, other mechanisms of interspecies electron transfer exist including cysteine cycling and possibly direct interspecies electron transfer as electric current via conductive pili or (semi)conductive minerals