Initiator tRNA Genes Template the 3′ CCA End at High Frequencies in Bacteria

While the CCA sequence at the mature 3 end of tRNAs is conserved and critical for translational function, a genetic template for this sequence is not always contained in tRNA genes. In eukaryotes and archaea, the CCA ends of tRNAs are synthesized post-transcriptionally by CCA-adding enzymes. In bacteria, tRNA genes template CCA sporadically. In order to understand variation in how prokaryotic tRNA genes template CCA, we re-annotated tRNA genes in the tRNAdb-CE database. Among 132,129 prokaryotic tRNA genes, initiator tRNA genes template CCA at the highest average frequency (74.1%) over all functional classes except selenocysteine and pyrrolysine tRNA genes (88.1% and 100% respectively). Across bacterial phyla and a wide range of genome sizes, many lineages exist in which predominantly initiator tRNA genes template CCA. Preferential retention of CCA in initiator tRNA genes evolved multiple times during reductive genome evolution in Bacteria. Also, in a majority of cyanobacterial and actinobacterial genera, predominantly initiator tRNA genes template CCA. We suggest that cotranscriptional synthesis of initiator tRNA CCA 3 ends can complement inefficient processing of initiator tRNA precursors, \"bootstrap\" rapid initiation of protein synthesis from a non-growing state, or contribute to an increase in cellular growth rates by reducing overheads of mass and energy to maintain nonfunctional tRNA precursors. More generally, CCA templating in structurally non-conforming tRNA genes can afford cells robustness and greater plasticity to respond rapidly to environmental changes and stimuli.