Parallel evolution of the genetic code in arthropod mitochondrial genomes

Abstract

The genetic code provides the translation table necessary to transform the information contained in DNA into the language of proteins. In this table, a correspondence between each codon and each amino acid is established: tRNA is the main adaptor that links the two. Although the genetic code is nearly universal, several variants of this code have been described in a wide range of nuclear and organellar systems, especially in metazoan mitochondria. These variants are generally found by searching for conserved positions that consistently code for a specific alternative amino acid in a new species. We have devised an accurate computational method to automate these comparisons, and have tested it with 626 metazoan mitochondrial genomes. Our results indicate that several arthropods have a new genetic code and translate the codon AGG as lysine instead of serine (as in the invertebrate mitochondrial genetic code) or arginine (as in the standard genetic code). We have investigated the evolution of the genetic code in the arthropods and found several events of parallel evolution in which the AGG codon was reassigned between serine and lysine. Our analyses also revealed correlated evolution between the arthropod genetic codes and the tRNA-Lys/-Ser, which show specific point mutations at the anticodons. These rather simple mutations, together with a low usage of the AGG codon, might explain the recurrence of the AGG reassignments.

Figure 1. Performance of the Codon Assignment Method

The number of assignments concordant (diamonds) and non-concordant (squares) with GenBank annotations, as well as the number of codons left unpredicted (because there were no observations for them; triangles) at different thresholds of entropy are shown.

Figure 2. Codon-Usage and Strength of Prediction

The number of codons used for each codon assignment and the frequency of the predicted amino acid are shown. Blue diamonds indicate assignments that are concordant with GenBank annotations; pink crosses, discordant assignments; and yellow triangles, discordant assignments where AGG is assigned to lysine.

Figure 3. Usage of the TCN and AGN Codons in the 24 Arthropod Mitochondrial Genomes Predicted to Translate AGG as Lys

The overall usage of the TCN/AGN codons (A), and their particular usage at protein sites where Ser (B) or Lys (C) are conserved across more than 80% of the 626 analyzed metazoan mtDNAs are shown. N=A, C, G, or T; H=A, C, or T.

Figure 4. Evolution of the Mitochondrial Genetic Code in Arthropods

This figure merges two independent most-parsimonious ancestral character state reconstructions: the presence (transparent) or absence (light grey) of the AGG codon, and the predicted translation of AGG as Lys (purple) or Ser (yellow). Species in which AGG was not predicted and species in which we determined that the assignment was unreliable (nodes without a rectangle) were treated as ambiguous states. The number of AGG codons, and the anticodons of tRNA-Lys and tRNA-Ser are indicated next to the species name.

Figure 5. The Molecules of tRNA-Lys and -Ser in Arthropods Having Either the AAMGC or the IMGC

The tRNA-Lys and -Ser anticodons in species decoding AGG as Lys or Ser, as well as the predicted translation of AGN and AAR mRNA-codons, are shown. Note that anticodons are depicted in 3′ to 5′ sense, i.e. UUC in tRNA-Lys corresponds to the anticodon CUU in standard notation.