Genome-Wide Analysis Reveals Ancestral Lack of Seventeen Different tRNAs and Clade-Specific Loss of tRNA-CNNs in Archaea

Transfer RNA (tRNA) is a category of RNAs that specifically decode messenger RNAs (mRNAs) into proteins by recognizing a set of 61 codons commonly adopted by different life domains. The composition and abundance of tRNAs play critical roles in shaping codon usage and pairing bias, which subsequently modulate mRNA translation efficiency and accuracy. Over the past few decades, effort has been concentrated on evaluating the specificity and redundancy of different tRNA families. However, the mechanism and processes underlying tRNA evolution have only rarely been investigated. In this study, by surveying tRNA genes in 167 completely sequenced genomes, we systematically investigated the composition and evolution of tRNAs in Archaea from a phylogenetic perspective. Our data revealed that archaeal genomes are compact in both tRNA types and copy number. Generally, no more than 44 different types of tRNA are present in archaeal genomes to decode the 61 canonical codons, and most of them have only one gene copy per genome. Among them, tRNA-Met was significantly overrepresented, with an average of three copies per genome. In contrast, the tRNA-UAU and 16 tRNAs with A-starting anticodons (tRNA-ANNs) were rarely detected in all archaeal genomes. The conspicuous absence of these tRNAs across the archaeal phylogeny suggests they might have not been evolved in the common ancestor of Archaea, rather than have lost independently from different clades. Furthermore, widespread absence of tRNA-CNNs in the Methanococcales and Methanobacteriales genomes indicates convergent loss of these tRNAs in the two clades. This clade-specific tRNA loss may be attributing to the reductive evolution of their genomes. Our data suggest that the current tRNA profiles in Archaea are contributed not only by the ancestral tRNA composition, but also by differential maintenance and loss of redundant tRNAs.