Oral Presentation Australian Society for Microbiology Annual Scientific Meeting 2021

Stop codon recoding enhances the metabolic capabilities of two novel methylotrophic Asgardarchaeota lineages (#139)

Jiarui Sun 1 , Paul Evans 1 , Emma Gagen 1 , Ben Woodcroft 2 , Brian Hedlund 3 , Tanja Woyke 4 , Philip Hugenholtz 1 , Christian Rinke 1
  1. Australian Centre for Ecogenomics, The University of Queensland, Brisbane, Queensland, Australia
  2. Queensland University of Technology, Brisbane, Queensland, Australia
  3. School of Life Sciences and Nevada Institute of Personalized Medicine, University of Nevada, Las Vegas, Nevada, USA
  4. DOE Joint Genome Institute, Walnut Creek, CA, USA

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 Hodurarchaeia class nov. and Cand. Jordarchaeia class nov., derived from the gods Hodur 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, allowing the incorporation of the rare 21st and 22nd amino acids selenocysteine (Sec) and pyrrolysine (Pyl). We found Sec-encoding system in Jordarchaeia and all other Asgardarchaeota classes, which likely benefit from increased catalytic activities of Sec-containing enzymes. Pyl-encoding system on the other hand is restricted to Hodurarchaeia 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.

  1. Rinke, C., et al. (2021). "Resolving widespread incomplete and uneven archaeal classifications based on a rank-normalized genome-based taxonomy." Nature Microbiology. (In press)