Abstract
Methanogenesis is the primary biogenic source of methane in the atmosphere and a key contributor to climate change. The long-standing dogma that methanogenesis originated within the Euryarchaeota was recently challenged by the discovery of putative methane-metabolizing genes in members of the Bathyarchaeota, suggesting that methanogenesis may be more phylogenetically widespread than currently appreciated. Here, we present the discovery of divergent methyl-coenzyme M reductase genes in population genomes recovered from anoxic environments with high methane flux that belong to a new archaeal phylum, the Verstraetearchaeota. These archaea encode the genes required for methylotrophic methanogenesis, and may conserve energy using a mechanism similar to that proposed for the obligate H2-dependent methylotrophic Methanomassiliicoccales and recently described Candidatus 'Methanofastidiosa'. Our findings indicate that we are only beginning to understand methanogen diversity and support an ancient origin for methane metabolism in the Archaea, which is changing our understanding of the global carbon cycle.
Highlights
Methanogenesis is the primary biogenic source of methane in the atmosphere and a key contributor to climate change
Discovery of a divergent mcrA cluster To enrich for novel methanogenic diversity, triplicate anaerobic digesters were inoculated with a mixture of samples sourced from natural and engineered environments, and supplied with alpha cellulose
This divergent mcrA was used to screen the Sequence Read Archive (SRA)[15], and closely related mcrA genes (85–100% aa identity, Supplementary Table 2) were identified in three metagenomic data sets obtained from high methane flux habitats: an anaerobic digester treating palm oil mill effluent (Malaysia)[16], an iso-alkane degrading methanogenic enrichment culture from tailings ponds (Mildred Lake Settling Basin, Canada)[17], and formation waters of coalbed methane wells (CD-8 and PK-28) located within the Surat Basin (Queensland, Australia)[12] (Supplementary Table 1)
Summary
Korarchaeota Aigarchaeota Terrestrial Hot Spring Crenarchaeota Group Crenarchaeota. V1; mesophilic anaerobic digester degrading cellulose C. Metabolic reconstruction of the near-complete Verstraetearchaeota genomes revealed the presence of key genes associated with methylotrophic methanogenesis (Figs 2b, 3a, and Supplementary Table 3). Digestus, form of digest, undergo digestion, pertaining to the anaerobic digester environment) This organism is inferred to be capable of methylotrophic methanogenesis, is non-motile, and not cultivated, represented by near-complete population genomes V1 (type strain) and V2 obtained from anaerobic digesters (Table 1). Carbo carbonis, coal, carbon, pertaining to the coalbed methane well environment) This organism is inferred to be capable of methylotrophic methanogenesis, is non-motile, and not cultivated, represented by population genomes V4 (near-complete) and V5 (moderately complete) obtained from formation water of coalbed methane wells (Table 1). Description of Verstraetearchaeota (phyl. nov.) We propose the name Verstraetearchaeota for this phylum; Verstraete, recognizing the contributions of Professor Willy Verstraete (Centre for Microbial Ecology and Technology, Ghent University, Belgium) to the development and application of engineered microbial ecosystems such as anaerobic digesters; suff. -archaeota, ending to denote an archaeal phylum
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