The sunlit microoxic niche of the archaeal eukaryotic ancestor comes to light

Abstract

Recent advances in phylogenomic analyses and increased genomic sampling of uncultured prokaryotic lineages brought compelling evidence in support of the emergence of eukaryotes from within the Archaea domain of life. The discovery of Asgardaeota archaea and their recognition as the closest extant relative of eukaryotes fuelled the revival of a decades-old debate regarding the topology of the tree of life. While it is apparent that Asgardaeota encode a plethora of eukaryotic-specific proteins (the highest number identified to date in prokaryotes), the lack of genomic information and metabolic characterization has precluded inferences about their lifestyles and the metabolic landscape that may have favoured the emergence of the hallmark eukaryotic subcellular architecture. Here, we use advanced phylogenetic analyses to infer the deep ancestry of eukaryotes and genome-scale metabolic reconstructions to shed light on the metabolic milieu of the closest archaeal eukaryotic ancestors discovered till date. In doing so, we: i) generate the largest Asgardaeota genomic dataset available so far, ii) describe a new clade of rhodopsins encoded within the recovered genomes, iii) provide unprecedented evidence for mixotrophy within Asgardaeota, iv) present first-ever proofs that the closest extant archaeal relatives to all eukaryotes (Heimdallarchaeia) have microoxic lifestyles with aerobic metabolic pathways unique among Archaea (i.e. kynurenine pathway) and v) generate the first images of Asgardaeota.