Metagenomic insights into the metabolism and evolution of a new Thermoplasmata order (Candidatus Gimiplasmatales)

Thermoplasmata is a widely distributed and ecologically important archaeal class in the phylum Euryarchaeota. Because few cultures and genomes are available, uncharacterized Thermoplasmata metabolisms remain unexplored. In this study, we obtained four medium- to high-quality archaeal metagenome-assembled genomes (MAGs) from the filamentous fragments of black-odorous aquatic sediments (Foshan, Guangdong, China). Based on their 16S rRNA gene and ribosomal protein phylogenies, the four MAGs belong to the previously unnamed Thermoplasmata UBA10834 clade. We propose that this clade (five reference genomes from the Genome Taxonomy Database (GTDB) and four MAGs from this study) be considered a new order, Candidatus Gimiplasmatales. Metabolic pathway reconstructions indicated that the Ca. Gimiplasmatales MAGs can biosynthesize isoprenoids and nucleotides de novo. Additionally, some taxa have genes for formaldehyde and acetate assimilation, and the Wood-Ljungdahl CO2-fixation pathway, indicating a mixotrophic lifestyle. Sulfur reduction, hydrogen metabolism, and arsenic detoxification pathways were predicted, indicating sulfur-, hydrogen-, and arsenic-transformation potentials. Comparative genomics indicated that the H4F Wood-Ljungdahl pathway of both Ca. Gimiplasmatales and Methanomassiliicoccales was likely obtained by the interdomain lateral gene transfer from the Firmicutes. Collectively, this study elucidates the taxonomic and potential metabolic diversity of the new order Ca. Gimiplasmatales and the evolution of this subgroup and its sister lineage Methanomassiliicoccales.

Automated summary

This study obtained four archaeal metagenome-assembled genomes (MAGs) from black-odorous aquatic sediments in Foshan, Guangdong, China, revealing the taxonomic and potential metabolic diversity of a new order Ca. Gimiplasmatales. The MAGs showed biosynthesis capabilities for isoprenoids and nucleotides, a mixotrophic lifestyle, and sulfur, hydrogen, and arsenic transformation potentials. Comparative genomics suggested that the H4F Wood-Ljungdahl pathway in Ca. Gimiplasmatales and Methanomassiliicoccales may have been acquired through interdomain lateral gene transfer from Firmicutes.