Final Report Summary - PUZZLE_CELL (Solving an evolutionary jigsaw puzzle: A next-generation genomics approach to trace the origins of the eukaryotic cell)
Ever since the recognition of the archaeal domain of life by Carl Woese and co-workers Archaea have featured prominently in hypotheses for the origin of eukaryotes, as eukaryotes and Archaea represented sister lineages in Woese’s ‘3 Domains Tree’ consisting of Bacteria, Archaea and Eukarya. Yet, alternative scenarios posit that the host cell emerged from within the archaeal domain, the so-called archaeal host or eocyte-like scenarios (‘2 Domains Tree’). Whereas Woese’s 3-Domain tree casted a long shadow on the field of eukaryogenesis during the 1990s and early 2000s, a number of phylogenetic studies in the late 2000s and early 2010s started reporting evidence for trees in which eukaryotes branched from within the archaeal domain of life. This all changed with our discovery of the Lokiarchaeota within the framework of this ERC project (Nature 521, pp 173-179). The detailed characterization of the first composite genome of the Lokiarchaeota provided several new insights into the archaeal origin of eukaryotes. Firstly, phylogenomic analyses of carefully selected genomic datasets placed Lokiarchaeota as the most closely related group to eukaryotes. Furthermore, a careful functional analysis of genome content of the composite Lokiarchaeum genome revealed that it encoded a multitude of genes that were previously regarded specific to eukaryotes. The discovery of Lokiarchaeota reignited debates about the very nature of the archaeal host cell from which eukaryotes emerged, leading to renewed hypotheses to explain the origin and early evolution of eukaryotes. Yet, it turned out that the discovery of Lokiarchaeota merely represented the tip of the iceberg, as a recent study reported on the existence of a group of uncultivated archaea that apart from Lokiarchaeota included Thor-, Odin- and Heimdallarchaeota (Nature 541, pp 353-358). This proposed archaeal superphylum, collectively referred to as Asgard archaea, affiliates with eukaryotes in phylogenomic analyses, and their genomes are enriched for proteins formerly considered being specific to eukaryotes. These findings significantly expanded the known repertoire of “eukaryote-specific” proteins in Archaea, indicating that the archaeal host cell already contained many key-components of the machineries that govern the compartmentalised nature of eukaryotic cells.