The ribosome is comprised of ribosomal RNA (rRNA) and ribosomal proteins (rProteins). The ribosomal common core includes the structurally conserved rRNA and rProtein of all species. The common core connects all life back to the Last Universal Common Ancestor (LUCA). In eukaryotes, the common core rRNA is elaborated with expansion segments (ESs), making the eukaryotic rRNA longer and more complex than bacterial or archaeal rRNA. The origin and evolution of ESs is a mystery and ESs over 100 nucleotides (supersized ESs) have not been previously observed in Bacteria or Archaea.
We show here that the large subunit (LSU) rRNA of two Asgard archaeal phyla, Lokiarchaeota and Heimdallarchaeota, is elaborated with supersized ES9 and ES39, bridging the gap in size between prokaryotic and eukaryotic LSU rRNA. The asgardian ESs connect to the universal common core rRNA at the same sites of attachment as the sites for eukaryotic and archaeal ES9 and ES39. These results suggest that the last Asgard and eukaryotic common ancestor (LAsECA) contained key components of the eukaryotic translational system. Although sequence conservation of ESs is low due to their high mutation rates, secondary and tertiary structures can be used to study ES homology and evolution. Computational covariation analysis and experimental chemical footprinting supports an mfold model of Lokiarchaeota ES39 structure. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE) is an experimental method that reveals the flexibility of RNA molecules. SHAPE demonstrated high flexibility for most unpaired nucleotides and low flexibility for most paired nucleotides of the modelled structure.
The evidence of µ-ESs in Archaea, ESs in Eukarya, and supersized ESs in Asgard species can be explained both by a two- or three-domain tree of life (TOL). By comparing the common eukaryotic ES39 signature fold with models for Asgard ES39s, we discovered that eukaryotic ES39s have longer unpaired regions than Lokiarchaeota and Heimdallarchaeota ES39s. Furthermore, we found a conserved three-way junction in Asgard ES39 that matches the eukaryotic ES39 topology. In a three-domain TOL model, a large ES39 in the Last Archaeal and Eukaryotic Common Ancestor (LAECA) could have been inherited in Asgard archaea and Eukarya without them necessarily being closely related. In a two-domain TOL model, the presence of similar three-way junction in Asgard and Eukarya ES39s corroborates the accretion model of ribosomal evolution, predicting a close relationship between Asgard archaea and Eukarya.
Penev, P. I., Fakhretaha-Aval, S., Patel, V. J., Cannone, J. J., Gutell, R. R., Petrov, A. S., Williams, L. D., & Glass, J. B. (2020). Supersized Ribosomal RNA Expansion Segments in Asgard Archaea. Genome biology and evolution, 12(10), 1694–1710. https://doi.org/10.1093/gbe/evaa170