Thermophilic archaea activate butane via alkyl-coenzyme M formation

Abstract

The anaerobic formation and oxidation of methane involve unique enzymatic mechanisms and cofactors, all of which are believed to be specific for C-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 C 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 C 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.

Microbial Community Response to Simulated Petroleum Seepage in Caspian Sea Sediments

“…Furthermore, only very few sequences (<<1% of total archaeal sequences) affiliated with other known methanogens such as Methanolobus and Methanococcoides (Methanosarcinaceae), Methanosaetaceae, Methanomicrobiaceae, Methanocellaceae, or Methermicoccaceae were detected in SOFT sediments (Supplementary Table S5). Methanotrophs of the ANME clades (ANME-1, ANME-2, ANME-3) and “ Candidatus Syntrophoarchaeum,” capable of anaerobic butane oxidation (Laso-Pérez et al, 2016) were only sporadically detected. In comparison, previous studies of the microbial community in Caspian Sea sediments identified Thaumarchaeota and Parvarchaeota as dominant in surface layers while Marine Benthic Group B (Lokiarchaeota) dominated the deeper layers (Mahmoudi et al, 2015).…”

Energy Metabolism during Anaerobic Methane Oxidation in ANME Archaea

“…M. nitroreducens”, gene loss may have been facilitated by the acquisition of nitrate and nitrite reductases from bacteria (35). Detailed phylogenetic and biochemical analyses of both the respiratory and C1-metabolizing enzymes in ANME will contribute to ordering the evolutionary events that resulted in the methane-oxidizing phenotype, particularly as our knowledge of organisms with methanogen-like genes and metabolism expands (28, 44, 56). It could be imagined that the ANME phenotype is one of many evolutionary trajectories away from what may have been an ancestral hydrogenotrophic methanogen phenotype (15, 75).…”

“…It is likely that in both acetate and methane metabolisms, continued studies will reveal a variety of subtle, yet critical differences in the enzyme modules harbored which allow these microbes to fill various ecological positions while retaining the core carbon pathways (see [44, 56] for recent findings). For both the methane forming and methane oxidizing archaea, a complete understanding of the enzyme compliments which underlie a given physiology is critical to evaluating ecological position and activity.…”

Diverse anaerobic methane‐ and multi‐carbon alkane‐metabolizing archaea coexist and show activity in Guaymas Basin hydrothermal sediment

“…These minority gases are usually present in variable amounts in seafloor sediments, ranging from traces to 30%-40% (Claypool and Kvenvolden, 1983;Welhan and Lupton, 1987;Ladygina et al, 2006). from the Euryarchaeota was reported to be capable of anaerobic oxidation of short-chain multi-carbon alkanes, namely, n-butane and propane, via methyl-coenzyme M reductase (MCR), the key enzyme in the (reverse) methanogenesis process (Laso-Pérez et al, 2016). Recently, an archaeal enrichment culture that primarily consisted of Ca.…”