The Evolutionary History of the Structure of 5S Ribosomal RNA
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5S rRNA is the smallest nucleic acid component of the large ribosomal subunit, contributing to ribosomal assembly, stability, and function. Despite being a model for the study of RNA structure and RNA–protein interactions, the evolution of this universally conserved molecule remains unclear. Here, we explore the history of the three-domain structure of 5S rRNA using phylogenetic trees that are reconstructed directly from molecular structure. A total of 46 structural characters describing the geometry of 666 5S rRNAs were used to derive intrinsically rooted trees of molecules and molecular substructures. Trees of molecules revealed the tripartite nature of life. In these trees, superkingdom Archaea formed a paraphyletic basal group, while Bacteria and Eukarya were monophyletic and derived. Trees of molecular substructures supported an origin of the molecule in a segment that is homologous to helix I (α domain), its initial enhancement with helix III (β domain), and the early formation of the three-domain structure typical of modern 5S rRNA in Archaea. The delayed formation of the branched structure in Bacteria and Eukarya lends further support to the archaeal rooting of the tree of life. Remarkably, the evolution of molecular interactions between 5S rRNA and associated ribosomal proteins inferred from a census of domain structure in hundreds of genomes established a tight relationship between the age of 5S rRNA helices and the age of ribosomal proteins. Results suggest 5S rRNA originated relatively quickly but quite late in evolution, at a time when primordial metabolic enzymes and translation machinery were already in place. The molecule therefore represents a late evolutionary addition to the ribosomal ensemble that occurred prior to the early diversification of Archaea.
KeywordsRibosome 5S rRNA Secondary structure Molecular evolution Cladistic analysis
We thank Ajith Harish for help with 3D mappings, Minglei Wang for calculating nd values, and Hee Shin Kim, Ajith Harish, Minglei Wang, Liudmila Yafremava, Kyung Mo Kim, and Jay Mittenthal for helpful discussions. This study was supported by National Science Foundation Grants MCB-0343126 and MCB-0749836, the Critical Research Initiative of the University of Illinois, and the United Soybean Board. Any opinions, findings, and conclusions and recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the funding agencies. Both authors designed and performed the experiments, analyzed the data, and wrote the article.
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