Timing the origin of eukaryotic cellular complexity with ancient duplications

Abstract

Eukaryogenesis is one of the most enigmatic evolutionary transitions, during which simple prokaryotic cells gave rise to complex eukaryotic cells 1,2 . The last eukaryotic common ancestor (LECA) harboured intracellular compartments, including mitochondria. In addition to mitochondrial endosymbiosis, eukaryogenesis was driven by numerous gene acquisitions 3 , inventions and duplications 4 , which shaped the ancestral eukaryotic traits. While evolutionary intermediates are lacking, gene duplications allow us to elucidate the order of events by which eukaryotes originated. Here we reconstruct successive steps during eukaryogenesis using phylogenomics and show that mitochondrial endosymbiosis was an intermediate episode. We found that gene duplications roughly doubled the proto-eukaryotic genome, with families inherited from the Asgard archaea-related host being duplicated most. Importantly, by relatively timing events using branch lengths we inferred that duplications of archaeal families occurred throughout eukaryogenesis, both before and after the acquisition of bacterial genes. Duplications in cytoskeletal and membrane trafficking families were among the earliest events, whereas most other families expanded primarily after mitochondrial endosymbiosis. Altogether, we demonstrate that the host that engulfed the protomitochondrion had some eukaryote-like complexity, which further increased drastically upon mitochondrial acquisition. This scenario bridges the signs of complexity observed in Asgard archaeal genomes 5,6 to the proposed role of mitochondria in triggering eukaryogenesis 7,8 .

The evolution of the Puf superfamily of proteins across the tree of eukaryotes

“…Indeed, as protoeukaryotes began to complexify, it is tempting to speculate that functional networks necessary to manage an expanding genome and gene repertoire would demand additional levels of regulation-a role potentially filled by RBPs such as the PufSF proteins. Future examination of the relative timing [52] of the emergence of PufSF proteins and their experimental characterization in diverse eukaryotic lineages will be critical in assessing these hypotheses.…”

Structure-based inference of eukaryotic complexity in Asgard archaea

“…For example, 64% of previously identified ESP clusters (336 of 425) have functions in cellular processing and signaling, including a hub of 59 clusters collectively encompassing 932 Asgard archaeal small GTPase protein representative structures (Fig. 3E), which are known to have undergone extensive duplication in both eukaryotes and Asgard archaea (10,11,21,35,36). In contrast, only 28% of iESP clusters (258 of 908) are involved in cellular processing and signaling functional (when including clusters containing multiple functional categories).…”