Shu, Wen-Sheng

AbstractSeveral recent studies have shown the presence of genes for the key enzyme associated with archaeal methane/alkane metabolism, methyl-coenzyme M reductase (Mcr), in metagenome-assembled genomes (MAGs) divergent to existing archaeal lineages. Here, we study the mcr-containing archaeal MAGs from several hot springs, which reveal further expansion in the diversity of archaeal organisms performing methane/alkane metabolism. Significantly, an MAG basal to organisms from the phylum Thaumarchaeota that contains mcr genes, but not those for ammonia oxidation or aerobic metabolism, is identified. Together, our phylogenetic analyses and ancestral state reconstructions suggest a mostly vertical evolution of mcrABG genes among methanogens and methanotrophs, along with frequent horizontal gene transfer of mcr genes between alkanotrophs. Analysis of all mcr-containing archaeal MAGs/genomes suggests a hydrothermal origin for these microorganisms based on optimal growth temperature predictions. These results also suggest methane/alkane oxidation or methanogenesis at high temperature likely existed in a common archaeal ancestor.

Abstract Several abundant but yet uncultivated bacterial groups exist in extreme iron- and sulfur-rich environments, and the physiology, biodiversity, and ecological roles of these bacteria remain a mystery. Here we retrieved four metagenome-assembled genomes (MAGs) from an artificial acid mine drainage (AMD) system, and propose they belong to a new deltaproteobacterial order, Candidatus Acidulodesulfobacterales. The distribution pattern of Ca. Acidulodesulfobacterales in AMDs across Southeast China correlated strongly with ferrous iron. Reconstructed metabolic pathways and gene expression profiles showed that they were likely facultatively anaerobic autotrophs capable of nitrogen fixation. In addition to dissimilatory sulfate reduction, encoded by dsrAB, dsrD, dsrL, and dsrEFH genes, these microorganisms might also oxidize sulfide, depending on oxygen concentration and/or oxidation reduction potential. Several genes with homology to those involved in iron metabolism were also identified, suggesting their potential role in iron cycling. In addition, the expression of abundant resistance genes revealed the mechanisms of adaptation and response to the extreme environmental stresses endured by these organisms in the AMD environment. These findings shed light on the distribution, diversity, and potential ecological role of the new order Ca. Acidulodesulfobacterales in nature.

Abstract Small acidophilic archaea belonging to Micrarchaeota and Parvarchaeota phyla are known to physically interact with some Thermoplasmatales members in nature. However, due to a lack of cultivation and limited genomes on hand, their biodiversity, metabolisms, and physiologies remain largely unresolved. Here, we obtained 39 genomes from acid mine drainage (AMD) and hot spring environments around the world. 16S rRNA gene based analyses revealed that Parvarchaeota were only detected in AMD and hot spring habitats, while Micrarchaeota were also detected in others including soil, peat, hypersaline mat, and freshwater, suggesting a considerable higher diversity and broader than expected habitat distribution for this phylum. Despite their small genomes (0.64–1.08 Mb), these archaea may contribute to carbon and nitrogen cycling by degrading multiple saccharides and proteins, and produce ATP via aerobic respiration and fermentation. Additionally, we identified several syntenic genes with homology to those involved in iron oxidation in six Parvarchaeota genomes, suggesting their potential role in iron cycling. However, both phyla lack biosynthetic pathways for amino acids and nucleotides, suggesting that they likely scavenge these biomolecules from the environment and/or other community members. Moreover, low-oxygen enrichments in laboratory confirmed our speculation that both phyla are microaerobic/anaerobic, based on several specific genes identified in them. Furthermore, phylogenetic analyses provide insights into the close evolutionary history of energy related functionalities between both phyla with Thermoplasmatales. These results expand our understanding of these elusive archaea by revealing their involvement in carbon, nitrogen, and iron cycling, and suggest their potential interactions with Thermoplasmatales on genomic scale.