Deciphering the Evolution of the Mitochondrial Genetic Code in Arthropods

Inside arthropod's mitochondria the AGG codon is translated differently by distinct species. In some species, AGG is translated as lysine (Lys), whereas in others the typical mitochondrial genetic code of invertebrates operates, and AGG is translated as serine (Ser). There are also arthropods that, instead of translating AGG as Lys or Ser, simply make no use of this codon. The reassignment of the translation of the AGG codon from Ser to Lys has never been observed outside this taxonomic group. The molecular basis of this reassignment lies on point mutations at the anticodons of tRNA (transfer ribonucleic acid)–Ser and tRNA–Lys. Decodification of the AGG codon by the tRNA–Lys (with a CUU anticodon) requires a unique wobble pairing at the second position. The low affinity between the AGG codon and the CUU anticodon most likely explains why tRNA–Ser dominates over tRNA–Lys when both are able to recognise AGG. Ancestral character state reconstruction suggests that the arthropod-specific genetic code variant (AGG=Lys) possibly was already present in the ancestor of arthropods, having reverted to the invertebrate character state (AGG=Ser) multiple times in different arthropod lineages. Key Concepts: The genetic code provides a translation table between the DNA and protein alphabets. A standard genetic code shared by all life domains exists, but there are many variants. Alternative genetic codes are frequently found in metazoan mitochondrial genomes, probably due to their small size and lack of several tRNAs. Arthropods encompass a unique variant in which the AGG codon is translated as lysine, instead of serine, which is the standard meaning of AGG in invertebrates. Some arthropods make no use of the AGG codon. Several events of codon reassignment and reversions have occurred in parallel along the arthropod lineages. The translation of the AGG codon as lysine implies an exceptional wobble pairing with the CUU anticodon at the second position (G::U). Keywords: arthropods; genetic code; mitochondria; parallel evolution; anticodon mutations; ancestral character state reconstruction; AGG codon; lysine; serine; tRNA