A third lineage with two-piece tmRNA.

tmRNA combines tRNA and mRNA properties and helps bacteria to cope with stalled ribosomes. Its termini normally pair in the tRNA domain, closing the mRNA portion into a looping domain. A striking variation is a two-piece form that effectively breaks open the mRNA domain loop, resulting from independent gene permutation events in alphaproteobacteria and cyanobacteria. Convergent evolution to a similar form in separate bacterial lineages suggests that loop-opening benefits tmRNA function. This argument is strengthened by the discovery of a third bacterial lineage with a loop-opened two-piece tmRNA. Whereas most betaproteobacteria have one-piece tmRNA, a permuted tmRNA gene was found for Dechloromonas aromatica and close relatives. Correspondingly, two tmRNA pieces were identified, at approximately equal abundance and at a level one-fifteenth that of ribosomes, a 189 nt mRNA piece and a 65 nt aminoacylatable piece. Together these pieces were active with purified Escherichia coli translational components, but not alone. The proposed secondary structure combines common tmRNA features differently from the structures of other two-piece forms. The origin of the gene is unclear; horizontal transfer may be indicated by the similarity of the tRNA domain to that from a cyanobacterial two-piece tmRNA, but such transfer would not appear simple since the mRNA domain is most similar to that of other betaproteobacteria.