Metagenomes from Coastal Marine Sediments Give Insights into the Ecological Role and Cellular Features of Loki- and Thorarchaeota

Abstract

The genomes of Asgard Archaea, a novel archaeal proposed superphylum, share an enriched repertoire of eukaryotic signature genes and thus promise to provide insights into early eukaryote evolution. However, the distribution, metabolisms, cellular structures, and ecology of the members within this superphylum are not well understood. Here we provide a meta-analysis of the environmental distribution of the Asgard archaea, based on available 16S rRNA gene sequences. Metagenome sequencing of samples from a salt-crusted lagoon on the Baja California Peninsula of Mexico allowed the assembly of a new Thorarchaeota and three Lokiarchaeota genomes. Comparative analyses of all known Lokiarchaeota and Thorarchaeota genomes revealed overlapping genome content, including central carbon metabolism. Members of both groups contained putative reductive dehalogenase genes, suggesting that these organisms might be able to metabolize halogenated organic compounds. Unlike the first report on Lokiarchaeota, we identified genes encoding glycerol-1-phosphate dehydrogenase in all Loki- and Thorarchaeota genomes, suggesting that these organisms are able to synthesize bona fide archaeal lipids with their characteristic glycerol stereochemistry.IMPORTANCE Microorganisms of the superphylum Asgard Archaea are considered to be the closest living prokaryotic relatives of eukaryotes (including plants and animals) and thus promise to give insights into the early evolution of more complex life forms. However, very little is known about their biology as none of the organisms has yet been cultivated in the laboratory. Here we report on the ecological distribution of Asgard Archaea and on four newly sequenced genomes of the Lokiarchaeota and Thorarchaeota lineages that give insight into possible metabolic features that might eventually help to identify these enigmatic groups of archaea in the environment and to culture them.

Keywords: Archaea; Lokiarchaeota; Thorarchaeota; ether lipids; eukaryotic evolution; reductive dehalogenase.

FIG 1

(A) 16S rRNA diversity of Asgard archaea based on representative gene sequences filtered from the SILVA database (v.132). Stars indicate full-length 16S rRNA gene sequences from publicly available genomes. Squares indicate full-length 16S rRNA gene sequences from genomes obtained in this study. In parentheses for each group is given the number of sequences used for calculating this refined phylogenetic tree (left) and the total number of sequences that we found being affiliated with it (right). Small triangles indicate bootstrap values of >85% (SH-aLRT). (B) Environmental distribution of Asgard archaea. (C) pH ranges of the environment from which genomes of Asgard group representatives have been found. Group representatives with a sequenced genome were recovered based on a literature survey.

FIG 2

Concatenated ribosomal protein tree of Asgard archaea (blue, Thorarchaeota; yellow, Odinarchaeota; green, Lokiarchaeota; and red, Heimdallarchaeota). Selected representative archaeal genomes from other phyla are shown in black. The maximum likelihood phylogeny was reconstructed in IQ-TREE with the LG+F+I+G4 model. The alignment was trimmed to 6,732 positions with the BMGE (Block Mapping and Gathering with Entropy) tool. Branch support is denoted by triangles with an SH-aLRT value of >85%.

FIG 3

Shared and specific Loki- and Thorarchaeota core genomes. The Venn diagram represents the shared orthogroups between the public Loki- and Thorarchaeota genomes together with the four genomes obtained from Baja California. Numbers in parentheses represent the number of group-specific orthogroups present in all Lokiarchaeota (5 genomes) or all Thorarchaeota (8 genomes). Numbers in the center indicate orthogroups present in all Loki- and Thorarchaeota (13 genomes [shared core genome]).

FIG 4

Presence/absence matrix of the different orthogroups in the different Loki- and Thorarchaeota genomes. The orthologous groups are sorted for each arCOG class from present in all 13 genomes to singletons (present in 1 genome). For better visualization, singletons belonging to the hypothetical protein ArCOG are not shown.

FIG 5

Maximum likelihood tree of the putative archaeal RDases and RDases with demonstrated activity (75). UniProt accession numbers are included following the species designation and the gene name. Bootstrap values are indicated at the nodes. Consensus conserved domain organizations among indicated groups are shown on the right as determined by NCBI CD search for pfam domains and SignalP 5.0 for TAT signals.

FIG 6

Lipid membrane biosynthesis predictions from all Loki- and Thorarchaeota genomes. The colored circles (green, Lokiarchaeota; blue, Thorachaeota) represent the presence or absence of the enzymes in the pathway. Colored circles with a black border represent the genomes from this study. The colored semicircle represents the predicted putative fragment of the G1PDH enzyme in Lokiarchaeota GC14. The predictions and pathways are based on a prior publication (40). G1P, glycerol-1-phosphate; G3P, glycerol-3-phosphate; DHAP, dihydroxyacetone phosphate; GGGP, geranylgeranylglyceryl phosphate; and DGGGP, digeranylgeranylglyceryl phosphate.