Initiator tRNA genes template the 3' CCA end at high frequencies in bacteria.

David H Ardell,Ya-Ming Hou

doi:10.1186/s12864-016-3314-x

Abstract

BackgroundWhile 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.ResultsIn order to understand the variation in how prokaryotic tRNA genes template CCA, we re-annotated tRNA genes in tRNAdb-CE database version 0.8. 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. Convergent and parallel retention of CCA templating in initiator tRNA genes evolved in independent histories of reductive genome evolution in Bacteria. Also, in a majority of cyanobacterial and actinobacterial genera, predominantly initiator tRNA genes template CCA. We also found that a surprising fraction of archaeal tRNA genes template CCA.ConclusionsWe 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 precursor pools. 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3314-x) contains supplementary material, which is available to authorized users.

Highlights

While the CCA sequence at the mature 3′ end of transfer ribonucleic acid (tRNA) is conserved and critical for translational function, a genetic template for this sequence is not always contained in tRNA genes
Exceptions are found in Bacteria, where some tRNA genes contain a template of the CCA sequence for direct synthesis at the time of transcription
The Proteobacterial model for the tRNAICleAU elongator class that comes with The "tRNA Family" tRNA function classifier (TFAM) 1.4 does not generalize well to all bacterial phyla [13]

Summary

Introduction

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. One source of error in the annotation of tRNA genes concerns the functional classification of genes for tRNAs with CAU anticodons These include genes for initiator tRNAfMet, elongator tRNAMet and elongator tRNAICleAU isoacceptors that read AUA codons in Bacteria and Archaea. In this last case of elongator tRNAICleAU, the cytidines at the wobble anticodon position 34 (of the Sprinzl coordinate system for tRNA structure [4]) in transcribed CAU anticodons (C34) are post-transcriptionally modified to lysidine in most Bacteria [5, 6], changing the decoding specificity of these tRNAs from AUG to AUA codons. This alternative model is imperfect in its sensitivity and specificity [12], as discussed further below, its performance is satisfactory and suitable for the present study

Methods

Results

Discussion

Conclusion