Expanding diversity of Asgard archaea and the elusive ancestry of eukaryotes

Abstract

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 'eukaryome' 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.

The asgardarchaeal-unique contribution to protein families of the eukaryotic common ancestor was 0.3%

“…Our analysis confirms a patchy distribution of ESPs among asgardarchaea (Dacks et al 2016, Zaremba-Niedzwiedzka et al 2017, Imachi et al 2020, Liu et al 2020, Klinger et al 2016, Inoue et al 2020, Bulzu et al 2019) (Fig. 1).…”

“…To begin with, the iconic tree that introduced three aboriginal lineages (Woese and Fox 1977) might require a revision. Phylogenomic analysis of asgardarchaea provides evidence for a two-domains tree and the emergence of the host cell lineage of eukaryogenesis from within the archaeal domain (Cox et al 2008, McInerney et al 2014, Hug et al 2016, Williams et al 2020) with some skepticism, however, remaining (Forterre 2015, Da Cunha et al 2018, Liu et al 2020). Parallel to the discovery of the asgardarchaea were immediate speculations regarding their cellular complexity (Dacks et al 2016, Pittis and Gabaldón 2016, Rout and Field 2017, Akil and Robinson 2018, Zachar et al 2018, Neveu et al 2020) and a faith of having identified the missing link between pro- and eukaryotic biology based on the identification of a few e ukaryote s ignature p roteins (ESPs), that we find to be only 27 on average.…”

“…Considering the amount of data gathered in just the few years (Imachi et al 2020, Liu et al 2020, Klinger et al 2016, Inoue et al 2020, Bulzu et al 2019, Villanueva et al 2016), it is surprising asgardarchaea have escaped identification for so long. Their habitats had been sampled before, so it is likely that the method used and maybe an obligate dependency on syntrophy, hindered culturing except for one imposing exception (Imachi et al 2020).…”

The tree of life describes a tripartite cellular world

“…[18,19] Similarly, a recent study that significantly expanded Asgard diversity by sampling novel lineages also preferentially produced 3D trees when employing a range of sequence evolution models. [20] Despite these mixed results and underlying uncertainties in phylogenetic reconstruction, and the fact that the majority of Asgard genomes are derived from metagenome assemblies, several scientists claim that the 2D ToL model has now replaced the 3D model, contending that the debate is now settled. [13,21] Others argue the debate remains open [18][19][20]22] or support an alternative 2D tree with eukaryotes and prokaryotes as the two primary superkingdoms.…”

“…[20] Despite these mixed results and underlying uncertainties in phylogenetic reconstruction, and the fact that the majority of Asgard genomes are derived from metagenome assemblies, several scientists claim that the 2D ToL model has now replaced the 3D model, contending that the debate is now settled. [13,21] Others argue the debate remains open [18][19][20]22] or support an alternative 2D tree with eukaryotes and prokaryotes as the two primary superkingdoms. [23] Here, we revisit the 3D versus 2D debate.…”