Parallel Loss of Nuclear-Encoded Mitochondrial Aminoacyl-tRNA Synthetases and mtDNA-Encoded tRNAs in Cnidaria

Abstract

Unlike most animal mitochondrial (mt) genomes, which encode a set of 22 transfer RNAs (tRNAs) sufficient for mt protein synthesis, those of cnidarians have only retained one or two tRNA genes. Whether the missing cnidarian mt-tRNA genes relocated outside the main mt chromosome or were lost remains unclear. It is also unknown what impact the loss of tRNA genes had on other components of the mt translational machinery. Here, we explored the nuclear genome of the cnidarian Nematostella vectensis for the presence of mt-tRNA genes and their corresponding mt aminoacyl-tRNA synthetases (mt-aaRS). We detected no candidates for mt-tRNA genes and only two mt-aaRS orthologs. At the same time, we found that all but one cytosolic aaRS appear to be targeted to mitochondria. These results indicate that the loss of mt-tRNAs in Cnidaria is genuine and occurred in parallel with the loss of nuclear-encoded mt-aaRS. Our phylogenetic analyses of individual aaRS revealed that although the nearly total loss of mt-aaRS is rare, aaRS gene deletion and replacement have occurred throughout the evolution of Metazoa.

Genetic aspects of mitochondrial genome evolution

“…In most cases, there are missing or additional genes, most frequently a loss of tRNA genes. In diploblasts, the deletion of many or even most tRNAs is a common phenomenon (Haen et al, 2010;Wang and Lavrov, 2008). Among protostomes, in particular Rotifera (Suga et al, 2008) and Onychophora (Braband et al, 2010) are affected.…”

Identity elements for the aminoacylation of metazoan mitochondrial tRNAArghave been widely conserved throughout evolution and ensure the fidelity of the AGR codon reassignment

“…Cnidarians, that largely import both cytoplasmic tRNAs and their cognate synthetases to the mitochondria, 50 have retained the conventional arginine codons in the mitochondrial genome.…”

Insights into the transcriptional and translational mechanisms of linear organellar chromosomes in the box jellyfish Alatina alata (Cnidaria: Medusozoa: Cubozoa)

“…Previous studies have suggested that the loss of mt-tRNAs preceded that of the corresponding mt-aaRSs in Cnidaria 43 ; cases where an mt-tRNA is present in the absence of the corresponding Figure 2. Secondary structure of the putative origin of translation (OT) found on all 8 chromosomes of the mt genome of Alatina alata using the DNA folding program from the mfold Web Server with default parameters.…”

“…This pattern is in accord with the evolutionary scenario of parallel loss of mttRNAs and mt-aaRS, excluding mt-PheRS, which is made of a single protein as opposed to nc-PheRS composed of 2 subunits encoded by 2 separate genes. 29,43 Three full transcripts (Glu/ ProRS, IleRS and ValRS) did not harbor a recognizable 5 0 mitochondrial-targeting signal peptide (Table 3), while the sequence for HisRS was missing the 5 0 end where the mt-targeting signal peptide is expected to be found. The absence of mt-targeting signal peptides in Glu/ProRS, IleRS and ValRS suggests some post-transcriptional modification that might be responsible for the transport of these nc-aaRSs into the mitochondrion, though the possibility of a deviant targeting signal not identified by the prediction programs cannot be ruled out.…”