Bathyarchaeota, formerly known as the Miscellaneous Crenarchaeotal Group, is a phylum of global generalists that are widespread in anoxic sediments, which host relatively high abundance archaeal communities. Until now, 25 subgroups have been identified in the Bathyarchaeota. The distinct bathyarchaeotal subgroups diverged to adapt to marine and freshwater environments. Based on the physiological and genomic evidence, acetyl-coenzyme A-centralized heterotrophic pathways of energy conservation have been proposed to function in Bathyarchaeota; these microbes are able to anaerobically utilize (i) detrital proteins, (ii) polymeric carbohydrates, (iii) fatty acids/aromatic compounds, (iv) methane (or short chain alkane) and methylated compounds, and/or (v) potentially other organic matter. Furthermore, bathyarchaeotal members have wide metabolic capabilities, including acetogenesis, methane metabolism, and dissimilatory nitrogen and sulfur reduction, and they also have potential interactions with anaerobic methane-oxidizing archaea, acetoclastic methanogens and heterotrophic bacteria. These results have not only demonstrated multiple and important ecological functions of this archaeal phylum, but also paved the way for a detailed understanding of the evolution and metabolism of archaea as such. This review summarizes the recent findings pertaining to the ecological, physiological and genomic aspects of Bathyarchaeota, highlighting the vital role of this phylum in global carbon cycling.
Methanogenesis and anaerobic methane oxidation through methyl-coenzyme M reductase (MCR) as a key enzyme have been suggested to be basal pathways of archaea 1 . How widespread MCR-based alkane metabolism is among archaea, where it occurs and how it evolved remain elusive. Here, we performed a global survey of MCR-encoding genomes based on metagenomic data from various environments. Eleven high-quality mcr-containing metagenomic-assembled genomes were obtained belonging to the Archaeoglobi in the Euryarchaeota, Hadesarchaeota and different TACK superphylum archaea, including the Nezhaarchaeota, Korarchaeota and Verstraetearchaeota. Archaeoglobi WYZ-LMO1 and WYZ-LMO3 and Korarchaeota WYZ-LMO9 encode both the (reverse) methanogenesis and the dissimilatory sulfate reduction pathway, suggesting that they have the genomic potential to couple both pathways in individual organisms. The Hadesarchaeota WYZ-LMO4-6 and Archaeoglobi JdFR-42 encode highly divergent MCRs, enzymes that may enable them to thrive on non-methane alkanes. The occurrence of mcr genes in different archaeal phyla indicates that MCR-based alkane metabolism is common in the domain of Archaea.Since the emergence of life on our planet, anaerobic methane metabolism, including methanogenesis and methane oxidation, has been a crucial element in the Earth's carbon cycle 1 , and both processes are key to the global methane budget. Methanogenic archaea produce ~500-600 Tg of methane per year 2 , whereas anaerobic methane-oxidizing archaea (ANME) oxidize a large portion of methane within the seafloor before it reaches the water column 3,4 . The metabolic pathways of methane formation and anaerobic oxidation of methane are largely identical, as both contain exclusively C 1 -compound-transforming enzymes that were described originally in the methanogenesis pathway [5][6][7] .Among these enzymes, methyl-coenzyme M (CoM) reductase (MCR) plays the crucial role 8 . In methanogens, MCR reduces CH 3 -CoM to CH 4 (refs. 9,10 ), whereas in ANMEs, this enzyme activates CH 4 to form CH 3 -CoM as the primary intermediate 5 . This canonical MCR type is highly conserved, and the gene encoding the α-subunit (mcrA) of the enzyme complex has been used as a diagnostic marker for the detection and phylogenetic classification of methanogens and ANMEs 11 . The presence of MCR was thought to be limited to the phylum Euryarchaeota, yet the occurrence of mcr genes in metagenome-assembled genomes (MAGs) of the Bathyarchaeota 12 and Verstraetearchaeota 13 has indicated a much wider distribution of this gene within archaea. In addition, highly divergent MCR types have been identified in two strains of the thermophilic Ca. Syntrophoarchaeum spp. that use the encoded enzymes to activate
The Miscellaneous Crenarchaeota group (MCG) Archaea is one of the predominant archaeal groups in anoxic environments and may have significant roles in the global biogeochemical cycles. However, no isolate of MCG has been cultivated or characterized to date. In this study, we investigated the genetic organization, ecophysiological properties and evolutionary relationships of MCG archaea with other archaeal members using metagenome information and the result of gene expression experiments. A comparison of the gene organizations and similarities around the 16S rRNA genes from all available MCG fosmid and cosmid clones revealed no significant synteny among genomic fragments, demonstrating that there are large genetic variations within members of the MCG. Phylogenetic analyses of large-subunit+small-subunit rRNA, concatenated ribosomal protein genes and topoisomerases IB gene (TopoIB) all demonstrate that MCG constituted a sister lineage to the newly proposed archaeal phylum Aigarchaeota and Thaumarchaeota. Genes involved in protocatechuate degradation and chemotaxis were found in a MCG fosmid 75G8 genome fragment, suggesting that this MCG member may have a role in the degradation of aromatic compounds. Moreover, the expression of a putative 4-carboxymuconolactone decarboxylase was observed when the sediment was supplemented with protocatechuate, further supporting the hypothesis that this MCG member degrades aromatic compounds.
Members of the archaeal phylum are among the most abundant microorganisms on Earth. Although versatile metabolic capabilities such as acetogenesis, methanogenesis, and fermentation have been suggested for bathyarchaeotal members, no direct confirmation of these metabolic functions has been achieved through growth of in the laboratory. Here we demonstrate, on the basis of gene-copy numbers and probing of archaeal lipids, the growth of subgroup Bathy-8 in enrichments of estuarine sediments with the biopolymer lignin. Other organic substrates (casein, oleic acid, cellulose, and phenol) did not significantly stimulate growth of Meanwhile, putative bathyarchaeotal tetraether lipids incorporated C fromC-bicarbonate only when added in concert with lignin. Our results are consistent with organoautotrophic growth of a bathyarchaeotal group with lignin as an energy source and bicarbonate as a carbon source and shed light into the cycling of one of Earth's most abundant biopolymers in anoxic marine sediment.
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