Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen

Abstract

The ecophysiology of one candidate methanogen class WSA2 (or Arc I) remains largely uncharacterized, despite the long history of research on Euryarchaeota methanogenesis. To expand our understanding of methanogen diversity and evolution, we metagenomically recover eight draft genomes for four WSA2 populations. Taxonomic analyses indicate that WSA2 is a distinct class from other Euryarchaeota. None of genomes harbor pathways for CO 2 -reducing and aceticlastic methanogenesis, but all possess H 2 and CO oxidation and energy conservation through H 2 -oxidizing electron confurcation and internal H 2 cycling. As the only discernible methanogenic outlet, they consistently encode a methylated thiol coenzyme M methyltransferase. Although incomplete, all draft genomes point to the proposition that WSA2 is the first discovered methanogen restricted to methanogenesis through methylated thiol reduction. In addition, the genomes lack pathways for carbon fixation, nitrogen fixation and biosynthesis of many amino acids. Acetate, malonate and propionate may serve as carbon sources. Using methylated thiol reduction, WSA2 may not only bridge the carbon and sulfur cycles in eutrophic methanogenic environments, but also potentially compete with CO 2 -reducing methanogens and even sulfate reducers. These findings reveal a remarkably unique methanogen 'Candidatus Methanofastidiosum methylthiophilus' as the first insight into the sixth class of methanogens 'Candidatus Methanofastidiosa'.

Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis

“…In the present phylogenetic analysis that used different protein sets and methods, AMET1/HMET1, Methanomasilliicoccales 13 , ANME1 group 44 and ‘ Candidatus Methanofastidiosa’ (WSA2 group) 21 clustered together with high confidence (Supplementary Figure 9 and 10, Supplementary Data 2, 3 and 4). This topology differs from the topology of the ribosomal protein tree (Figure 4a).…”

Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota

“…Although HdrD is conventionally linked to HdrE (ref. 2), the latter is missing from the genomes, an observation that has also been made for the Methanomassiliicoccales 9 , C. 'Methanofastidiosum methylthiophilus' 10 and Bathyarchaeota 12 . Instead, HdrD may interact directly with the Fpo-like complex and together function as an energy-converting ferredoxin:heterodisulfide oxidoreductase 5 .…”

“…Similar to Methanomassiliicoccales 5,9 and Methanosaeta thermophila 21 , the subunits required for binding and oxidation of NADH (NuoEFG) or F 420 (FpoFO) are missing from the Verstraetearchaeota, supporting the use of ferredoxin as an electron donor. Reduced ferredoxin can also be re-oxidized by the energy-conserving hydrogenase B (Ehb) found in all genomes, as suggested for Methanosphaera stadtmanae 1 and the recently described C. 'Methanofastidiosum methylthiophilus' 10 .…”

“…Our knowledge of methanogenic substrate utilization and energy conservation is still incomplete but is rapidly expanding through the development of new molecular techniques such as genome-centric metagenomics. This includes the discovery of hydrogenotrophic methanogenesis genes encoded in Methanosaeta 8 , a genus originally thought to be strictly acetoclastic, the hypothesized mode of energy metabolism in Methanonomassiliiccocales 5,9 , and the recently described sixth class of euryarchaeotal methanogens, Candidatus 'Methanofastidiosa', which is restricted to methanogenesis through methylated thiol reduction 10 . The hypothesis that methane metabolism originated early in the evolution of the Euryarchaeota 11 has recently been challenged following the discovery of putative methane metabolism in the archaeal phylum Bathyarchaeota (formerly Miscellaneous Crenarchaeota Group) 12,13 .…”

Genomic composition and dynamics amongMethanomicrobialespredict adaptation to contrasting environments

“…Methanogens consist of at least nine (Mihajlovski et al, 2008;Sakai et al, 2008;Evans et al, 2015;Nobu et al, 2016) recognized orders and are divided into two major categories based on whether or not they contain cytochromes. Methanogens of the Methanosarcinales order contain cytochromes and use substrates such as acetate, methanol, methylamines and H 2 /CO 2 .…”