Methyl/alkyl‐coenzyme M reductase‐based anaerobic alkane oxidation in archaea

Abstract

Methyl-coenzyme M reductase (MCR) has been originally identified to catalyse the final step of the methanogenesis pathway. About 20 years ago anaerobic methane-oxidizing archaea (ANME) were discovered that use MCR enzymes to activate methane. ANME thrive at the thermodynamic limit of life, are slow-growing, and in most cases form syntrophic consortia with sulfate-reducing bacteria. Recently, archaea that have the ability to anaerobically oxidize non-methane multi-carbon alkanes such as ethane and n-butane were described in both enrichment cultures and environmental samples. These anaerobic multi-carbon alkane-oxidizing archaea (ANKA) use enzymes homologous to MCR named alkyl-coenzyme M reductase (ACR). Here we review the recent progresses on the diversity, distribution and functioning of both ANME and ANKA by presenting a detailed MCR/ACRbased phylogeny, compare their metabolic pathways and discuss the gaps in our knowledge of physiology of these organisms. To improve our understanding of alkane oxidation in archaea, we identified three directions for future research: (i) expanding cultivation attempts to validate omics-based metabolic models of yet-uncultured organisms, (ii) performing biochemical and structural analyses of key enzymes to understand thermodynamic and steric constraints and (iii) investigating the evolution of anaerobic alkane metabolisms and their impact on biogeochemical cycles.

Thermogenic hydrocarbon biodegradation by diverse depth-stratified microbial populations at a Scotian Basin cold seep

“…Depth profiles showed that bacteria capable of degrading liquid alkane and aromatic hydrocarbons were mainly detected in sulfate-depleted sediments, suggesting that they mediated hydrocarbon metabolism as part of methanogenic alkane-degrading consortia 8,44,45 . Also as expected, ANME-1 were found to be most abundant at the apparent sulfate-methane transition zone, in agreement with the well-documented syntrophy between methane-oxidizing archaea and sulfate-reducing bacteria in such settings 22 . These findings support that the cooperation of key bacterial and archaea hydrocarbon degraders with their partners is important for hydrocarbon degradation at deep sea cold seep sediments.…”

“…Syntrophoarchaeum and Desulfobacteraceae BuS5) 9,19 , dodecane (e.g., Desulfosarcina/Desulfococcus clade) 6 , and naphthalene (e.g., deltaproteobacterial strain NaphS2) 20,21 . Alkane-oxidizing archaea normally do so in consortia with sulfate-reducing bacteria whereas bacteria known to degrade hydrocarbons usually couple this to sulfate reduction in a single-cell process 8,22 . Long-chain alkanes can also be metabolized in syntrophic partnerships, e.g., by bacteria in the genera Smithella and Syntrophus, together with methanogenic archaea 23,24 .…”

Metagenomic Profiling and Microbial Metabolic Potential of Perdido Fold Belt (NW) and Campeche Knolls (SE) in the Gulf of Mexico

“…WLP is commonly found in acetogenic bacteria, archaea and recently has been found in non-methanogenic and non-methylotrophic archaea and bacteria, where its function remains unclear in the absence of methyl-coenzyme M reductase complex (MCR) and N5 -Methyltetrahydromethanopterin:coenzyme M methyltransferase complex (MTR) complexes ( Borrel et al, 2016 ; Chistoserdova, 2016 ); it has been suggested that it could be involved in other processes than methanogenesis like extra H2 production during fermentation or formaldehyde detoxification ( Adam et al, 2019 ). Recently, methanogenesis has been linked to alkane degradation through a divergent MCR within some Euryarchaeota capable of degrading ethane ( Chen et al, 2019 ; Laso-Pérez et al, 2019 ; Wang et al, 2020 ), which opens the possibility of having methanogens degrading hydrocarbons with MCRs not detected by this study.…”

Functional potential and assembly of microbes from sediments in a lake bay and adjoining river ecosystem for polycyclic aromatic hydrocarbon biodegradation

“…PAH degradation in the sediment is also limited by nutrient and electron acceptor availability, which can be improved by nutrient recycling and electron acceptor addition (Yan et al ., 2012; Yan et al ., 2014; Yan et al ., 2015; Yan et al ., 2017b; Wang et al ., 2020). PAHs can be degraded anaerobically under nitrate‐, iron‐, or sulfate‐reducing conditions (Lu et al ., 2012; Yan et al ., 2012; Ghattas et al ., 2017; Himmelberg et al ., 2018; Wang et al ., 2020). Anaerobic PAH degradation most likely occurred through mixed electron acceptor patterns in the RS.…”

“…Lake and adjoining river ecosystems are now increasingly threatened because they receive enormous quantities of organic matter (OM) and recalcitrant compounds such as polycyclic aromatic hydrocarbons (PAHs) (Zhao et al ., 2016; Tiegs et al ., 2019). Benthic microorganisms play a central role in the natural attenuation and bioremediation of PAH contamination from sediments (Acosta‐Gonzalez et al ., 2013; Himmelberg et al ., 2018; Yan et al ., 2019; Wang et al ., 2020). Moreover, the fate of PAHs in sediment environments depends strongly on microbial biodegradation potential (Yan et al ., 2012; Yan et al ., 2014; Yan et al ., 2017b).…”