Abstract
Transfer RNAs (tRNAs) are ancient molecules that are central to translation. Since they probably carry evolutionary signatures that were left behind when the living world diversified, we reconstructed phylogenies directly from the sequence and structure of tRNA using well-established phylogenetic methods. The trees placed tRNAs with long variable arms charging Sec, Tyr, Ser, and Leu consistently at the base of the rooted phylogenies, but failed to reveal groupings that would indicate clear evolutionary links to organismal origin or molecular functions. In order to uncover evolutionary patterns in the trees, we forced tRNAs into monophyletic groups using constraint analyses to generate timelines of organismal diversification and test competing evolutionary hypotheses. Remarkably, organismal timelines showed Archaea was the most ancestral superkingdom, followed by viruses, then superkingdoms Eukarya and Bacteria, in that order, supporting conclusions from recent phylogenomic studies of protein architecture. Strikingly, constraint analyses showed that the origin of viruses was not only ancient, but was linked to Archaea. Our findings have important implications. They support the notion that the archaeal lineage was very ancient, resulted in the first organismal divide, and predated diversification of tRNA function and specificity. Results are also consistent with the concept that viruses contributed to the development of the DNA replication machinery during the early diversification of the living world.
Highlights
Transfer RNA molecules are central to the entire translation process
We focus on transfer RNA, an ancient nucleic acid molecule that takes center stage in the process of protein biosynthesis and can be found everywhere in life
In a process that reconstructs history from molecular sequence and structure and at the same time forces molecules belonging to lineages into groups, we tested alternative hypotheses of origin and established when major organismal lineages appeared in evolution
Summary
They interact with the ribosomal RNA (rRNA) subunits as they are being ratcheted through the center of the ribosome [1,2] Their acceptor arms charge specific amino acids through the activity of cognate aminoacyl-tRNA synthetases, while triplets of bases on their ‘anticodon’ arms recognize complementary ‘codon’ sequences in messenger RNA. These and many other molecular interactions define the identities and functions of these tRNA adaptors and establish a genetic code that translates nucleic acid into protein information in the cell. Understanding phylogenetic trees is challenging because tRNA evolution embeds a history of recruitment in which structures gain or co-opt new identities and functions or takeover established ones
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