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

Abstract

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 blackodorous 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 CO 2fixation 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 H 4 F 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.

Continuous monocropping highly affect the composition and diversity of microbial communities in peanut (Arachis hypogaea L.)

“…The diversity of Nitrososphaerales was also reported from natural ecosystems and agricultural soil, where it was overrepresented in wet land and soil from tea plantations (Lynn et al, 2017). Thermoplasmata have a mixotrophic lifestyle that involves CO2 fixation as well as formaldehyde and acetate assimilation, and they have important potential functions in the carbon, sulfur, and arsenic processes (Hu et al, 2020). Thermoplasmata in our study showed decreased trends under consecutive monocropping, the abundance was higher in both T1and T2, which then decreased in T3 (Figure 4c).…”

The new archaeal order Lutiacidiplasmatales reveals convergent evolution in Thermoplasmatota

“…The selected topology largely agrees with the 16S rRNA gene phylogenetic tree (Figure S5). The Lutiacidiplasmatales order forms a monophyletic clade with the methanogenic Methanomassiliicoccales 34 and the recently described order-level groups Gimiplasmatales 13 , SG8-5 35 and Lunaplasmatales 10 (Figure 2).…”

“…Several contrasting evolutionary histories have been previously proposed for the Thermoplasmatota 5, 10, 13, 33 , particularly with the divergent placement of the clades Poseidoniales and Thermoprofundales. Therefore, our study provides an updated and robust phylogeny of the Thermoplasmatota (Figure 2).…”

“…Several novel groups of Thermoplasmatota have recently been described from a myriad of environments [10][11][12][13] . These genomes provide the opportunity to study the complex evolutionary history of this group, which has been proposed to be a critical model of complex archaeal evolution and adaptation to contrasted environments 5 .…”

Astrobiology of life on Earth

“…Within these genomes, Hu et al identify consistent groups of genes that could be capable of metabolizing complex organic compounds as well as de-novo synthesis of nucleic acids and mevalonate. Zhong et al (2021) report the expansion of accessory genes in the genomes of Thermococcales, and Hu et al (2021) provide evidence that one mechanism for such expansion is lateral gene transfer. The genomes of Candidatus Gimiplasmatales include genes for arsenic detoxification and cell motility.…”