Phylogenomic Analysis of Metagenome-Assembled Genomes Deciphered Novel Acetogenic Nitrogen-Fixing Bathyarchaeota from Hot Spring Sediments

We describe the Bathyarchaeota bins that are likely to be acetogens with a wide range of metabolic potential. These bins did not exhibit methanogenic machinery, suggesting methane production may not occur by all subgroup lineages of Bathyarchaeota. Phylogenetic analysis support that both ILS200 and ILS300 belonged to the Bathyarchaeota. The discovery of new bathyarchaeotal MAGs provides additional knowledge for understanding global carbon and nitrogen metabolism under extreme conditions. This study describes the phylogenomic analysis and metabolic insights of metagenome-assembled genomes (MAGs) retrieved from hot spring sediment samples. The metagenome-assembled sequences recovered three near-complete genomes belonging to the archaeal phylum. Analysis of genome-wide core genes and 16S rRNA-based phylogeny placed the ILS200 and ILS300 genomes within the uncultivated and largely understudied bathyarchaeal phylum, whereas ILS100 represented the phylum Thaumarchaeota. The average nucleotide identity (ANI) of the bin ILS100 was 76% with Nitrososphaeria_archaeon_isolate_SpSt-1069. However, the bins ILS200 and ILS300 showed ANI values of 75% and 70% with Candidatus_Bathyarchaeota_archaeon_isolate_DRTY-6_2_bin_115 and Candidatus_Bathyarchaeota_archaeon_BA1_ba1_01, respectively. The genomic potential of Bathyarchaeota bins ILS200 and ILS300 showed genes necessary for the Wood-Ljungdahl pathway, and the gene encoding the methyl coenzyme M reductase (mcr) complex essential for methanogenesis was absent. The metabolic potential of the assembled genomes included genes involved in nitrogen assimilation, including nitrogenase and the genes necessary for the urea cycle. The presence of these genes suggested the metabolic potential of Bathyarchaeota to fix nitrogen under extreme environments. In addition, the ILS200 and ILS300 genomes carried genes involved in the tricarboxylic acid (TCA) cycle, glycolysis, and degradation of organic carbons. Finally, we conclude that the reconstructed Bathyarchaeota bins are autotrophic acetogens and organo-heterotrophs. IMPORTANCE We describe the Bathyarchaeota bins that are likely to be acetogens with a wide range of metabolic potential. These bins did not exhibit methanogenic machinery, suggesting methane production may not occur by all subgroup lineages of Bathyarchaeota. Phylogenetic analysis support that both ILS200 and ILS300 belonged to the Bathyarchaeota. The discovery of new bathyarchaeotal MAGs provides additional knowledge for understanding global carbon and nitrogen metabolism under extreme conditions.

Automated summary

We described Bathyarchaeota bins with a wide range of metabolic potential, likely to be acetogens. Methane production may not occur in all subgroup lineages of Bathyarchaeota. The discovery of new bathyarchaeotal MAGs provides additional knowledge for understanding global carbon and nitrogen metabolism under extreme conditions.