The origin of eukaryotes represents an unresolved puzzle in evolutionary biology. For a long time, it was assumed that Archaea have played a central role in hypotheses on eukaryogenesis, and recent findings support the view that eukaryotes evolved from a symbiosis between an archaeal host and an alphaproteobacterial endosymbiont. The recent discovery of the Asgard superphylum, has shed additional light on this enigmatic event. Asgard archaea, whose genomes were obtained by metagenomics from various sediment samples across the world, represent the closest prokaryotic relatives of eukaryotes identified so far. Furthermore, their genomes harbor a plethora of eukaryotic signature proteins that may have been key in the evolution of complex eukaryotic cells. So far however, little is known about their metabolic potential and the evolution of their functional characteristics.
To unveil the metabolism of the elusive archaeal ancestor of eukaryotes, we have reconstructed the metabolism of Asgard archaea in a comparative genomics framework. Our analyses suggest, that the four different Asgard phyla, i.e. Odin-, Thor-, Loki- and Heimdallarchaeota are metabolically diverse and characterized by different metabolic lifestyles. While Thor- and Lokiarchaeota seem to be able to fix carbon via the Wood-Ljungdahl pathway and may be able to obtain energy from various organic substrates including fatty acids and perhaps hydrocarbons, Heimdallarchaeota seemingly encode terminal oxidases suggesting the ability to reduce nitrate or even oxygen. In contrast, Odinarchaeum might be a fermentative organism likely able to use H+ as electron acceptor. Altogether, our current analyses of these metabolic features and the reconstruction of the evolution of selected metabolic traits in the diversification of this superphylum show that previous inferences on the nature of the archaeal ancestor of eukaryotes need to be reconsidered and provide a more comprehensive basis for the formulation of an updated scenario on the evolution of eukaryotes from a metabolic point of view.