Expanding diversity of Asgard archaea and the elusive ancestry of eukaryotes

Comparative analysis of 162 (nearly) complete genomes of Asgard archaea, including 75 not reported previously, substantially expands the phylogenetic and metabolic diversity of the superphylum Asgard, with six additional phyla proposed. Phylogenetic analysis of universally conserved genes does not strongly support the origin of eukaryotes from within Asgard but rather, leans towards a three-domain topology, with eukaryotes branching outside archaea. Using sensitive methods for protein domains detection on the extended set of Asgard genomes results in a major expansion of the set of homologs of eukaryote signature proteins (ESPs). However, almost all Asgard ESPs show patchy phyletic distributions, large variations in the number of paralogs and variable domain architectures, suggestive of highly dynamic evolution via horizontal gene transfer (HGT), gene loss, gene duplication and domain shuffling. The results appear to be best compatible with an evolutionary scenario in which the conserved core of eukaryote genes involved in informational processes originates from an as yet unknown ancestral lineage deep within or outside the currently characterized archaeal diversity. Such hypothetical ancestors could have accumulated components of the mobile archaeal 9eukaryome9 via extensive HGT, eventually, giving rise to eukaryote-like cells. Our reconstruction of the metabolic networks for the extant and ancestral Asgard archaea reveals three distinct lifestyles, anaerobic heterotrophy, facultative aerobic heterotrophy, and chemolithotrophy, and suggests that the common ancestor of Asgard archaea was an acetogenic myxotroph capable of both production and consumption of hydrogen. These findings could be best compatible with different versions of the syntrophic hypothesis for eukaryogenesis, depending on the exact relationship between Asgard and eukaryotes.