Evolutionary Patterns in the Sequence and Structure of Transfer RNA: Early Origins of Archaea and Viruses

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.

Origins and evolution of modern biochemistry: insights from genomes and molecular structure

“…We also focused on tRNA, a molecule that bridges fundamental components of the translation machinery (94,138,139). tRNA is an adaptor with an acceptor arm (Acc) that charges amino acids through the specific activity of aminoacyl-tRNA synthetases and an anticodon (AC) arm with triplets of bases that recognize complementary codon sequences in mRNA.…”

“…Because tRNA phylogenies did not reveal clearly the tripartite nature of life or clear patterns linked to anticodon or amino acid-charging functions, we used phylogenetic constraint to untangle confounding histories of recruitment in these molecules (139). We forced tRNA molecules into monophyletic groups in the trees to falsify competing hypotheses and generated timelines of amino acid charging specificities, codon discovery, and organismal diversification.…”

Evolution of initiator tRNAs and selection of methionine as the initiating amino acid

“…18 Not surprisingly, when we constructed a tree with the minihelix regions of 2758 sequences of all tRNAs from a large variety of species, the results were too complicated for a clear understanding (data Figure 1. Phylogenetic tree using alignments of different segments of tRNA i sequence: The phylogenetic tree obtained using tRNA i sequences from different organisms from, (a) the whole tRNA i sequences, (b) the region having anticodon and DHU arm, and (c) the region having the acceptor and TcC arm.…”

“…S1), originated separately, and then over the course of evolution converged into a single entity. [13][14][15][16] The monophyletic theory of tRNA origin has been considered to derive tRNA phylogenies, 17,18 and while this method discerns 2 distinct classes (class I and class II) of tRNAs, it neither allows to clearly trace the ancestors of the different tRNAs nor their segregation into the 3 domains of life. 19 However, the polyphyletic theory of tRNA evolution has been preferred by a large number of studies.…”

Pragmatic turn in biology: From biological molecules to genetic content operators

“…Simple self-ligating RNA stem loops can build much larger groups of RNA stem loops that serve to increase complexity [66] . This may lead to ribozymatic consortia, which later on build success stories, such as the merger of the two subunits of transfer RNAs or RNA-dependent RNA-polymerases for replication of RNA through RNA or the subunits of ribosomal RNAs, all of them being former groups that evolved and functioned for different reasons than those applicable to subsequent conserved modes [67][68][69] . If RNA fragments self-ligate into self-replicating ribozymes they constitute networks.…”