Recoding enhances the metabolic capabilities of two novel methylotrophic Asgardarchaeota lineages

Abstract

Asgardarchaeota have been proposed as the closest living relatives to eukaryotes, and a total of 72 metagenome-assembled genomes (MAGs) representing six primary lineages in this archaeal phylum have thus far been described. These organisms are predicted to be fermentative organoheterotrophs contributing to carbon cycling in sediment ecosystems. Here, we double the genomic catalogue of Asgardarchaeota by obtaining 71 MAGs from a range of habitats around the globe, including deep subsurface, shallow lake, and geothermal spring sediments. Phylogenomic inferences followed by taxonomic rank normalisation confirmed previously established Asgardarchaeota classes and revealed four novel lineages, two of which were consistently recovered as monophyletic classes. We therefore propose the names Candidatus Hodarchaeia class nov. and Cand. Jordarchaeia class nov., derived from the gods Hod and Jord in Norse mythology. Metabolic inference suggests that both novel classes represent methylotrophic acetogens, encoding the transfer of methyl groups, such as methylated amines, to coenzyme M with acetate as the end product in remnants of a methanogen-derived core metabolism. This inferred mode of energy conservation is predicted to be enhanced by genetic code expansions, i.e. recoding, allowing the incorporation of the rare 21st and 22nd amino acids selenocysteine (Sec) and pyrrolysine (Pyl). We found Sec recoding in Jordarchaeia and all other Asgardarchaeota classes, which likely benefit from increased catalytic activities of Sec-containing enzymes. Pyl recoding on the other hand is restricted to Hodarchaeia in the Asgardarchaeota, making it the first reported non-methanogenic lineage with an inferred complete Pyl machinery, likely providing this class with an efficient mechanism for methylamine utilisation. Furthermore, we identified enzymes for the biosynthesis of ester-type lipids, characteristic of Bacteria and Eukaryotes, in both novel classes, supporting the hypothesis that mixed ether-ester lipids are a shared feature among Asgardarchaeota.

The expanding Asgard archaea and their elusive relationships with Eukarya

“…S1 in Da Cunha et al 5 ). This raises the possibility that the variable positions of 13 and Xie et al 14 , respectively, and in grey new lineages not present in these publications corresponding to the Sifarchaea 12 , the Jordarchaeia 16 and Asgard Lake Cootharaba 16 . The schema was designed combining the trees of all these publications.…”

“…The number of proposed Asgard phyla has continuously increased in recent years, from 1 in 2015 (Lokiarchaeota) to 18 in late 2021 (Figure 2 ) 1 , 2 , 10 , 11 , 12 , 13 , 14 , 15 , 16 . In a recent study, Liu et al 13 described six new Asgard phyla from an analysis of 75 metagenome‐assembled genomes (MAGs), while three additional phyla were described by Xie et al 14 from an analysis of 128 new MAGs.…”

“… Schematic representation of the known diversity of the Asgard archaea including the recently published lineages. In this schema, we indicate in orange and red the newly discovered lineages introduced in the two publications of Liu et al 13 and Xie et al 14 , respectively, and in grey new lineages not present in these publications corresponding to the Sifarchaea 12 , the Jordarchaeia 16 and Asgard Lake Cootharaba 16 . The schema was designed combining the trees of all these publications.…”

“…Rinke and colleagues recently proposed to consider the whole Asgard clade as a single phylum and the various Asgard lineages either as families or orders, with some of them being grouped in classes 16 . Since it is still an ongoing debate at the time of writing this review 18 , we will here use the more neutral term “lineage” for the various subgroups of Asgards (e.g., Heimdall lineage for Heimdallarchaeota/ales).…”

A closed Candidatus Odinarchaeum genome exposes Asgard archaeal viruses

“…Asgard archaea are a diverse group of microorganisms that comprise the closest relatives of eukaryotes [1][2][3][4][5][6][7] . Their genomes were first explored over six years ago 8 , and much of their physiology and cell biology remains to be studied.…”