Ancestry of RNA/RNA interaction regions within segmented ribosomes

Abstract

The ribosome is the universally conserved ribozyme that translates DNA coded instructions into proteins with the assistance of other RNA molecules, including transfer and messenger RNAs. Of particular interest is the segmentation phenomena, which is found in trypanosomatids and other protists. In these organisms, the large subunit ribosomal RNA is assembled from multiple smaller RNAs. This phenomenon posits several challenges to the folding and stabilization of such ribosomes to retain functionality and efficiency. In earlier studies, RNA/protein interactions were suggested to fully compensate for the fragmentation. Recently, several conserved RNA/RNA interaction regions were described in the cryo-EM structures of segmented ribosomes from trypanosomatids. These regions also seemed to aid in the folding and stabilization of such ribosomes, even before the ribosomal proteins start their association. In the present study, the existence of conserved RNA/RNA interaction regions shared between trypanosomatid andEuglena gracilissegmented ribosomes was confirmed, despite differences in segmentation patterns. Analysis of the crystallographic structures of unsegmented ribosomes from other Eukaryotes, Bacteria, and Archaea allowed us to estimate the relative age of highly conserved RNA/RNA interaction regions. These results strongly suggest that common interaction regions likely date far back into the ribosomes of the last common ancestor. Results also revealed that single hydrogen bonds are overwhelmingly facilitated by the 2′OH, a distinctive RNA feature. This supports the notion that RNA predates DNA and places some constraints on alternative nucleic acids proposals.