Coadaptation of isoacceptor tRNA genes and codon usage bias for translation efficiency in Aedes aegypti and Anopheles gambiae

Abstract

The transfer RNAs (tRNAs) are essential components of translational machinery. We determined that tRNA isoacceptors (tRNAs with different anticodons but incorporating the same amino acid in protein synthesis) show differential copy number abundance, genomic distribution patterns and sequence evolution between Aedes aegypti and Anopheles gambiae mosquitoes. The tRNA-Ala genes are present in unusually high copy number in the Ae. aegypti genome but not in An. gambiae. Many of the tRNA-Ala genes of Ae. aegypti are flanked by a highly conserved sequence that is not observed in An. gambiae. The relative abundance of tRNA isoacceptor genes is correlated with preferred (or optimal) and nonpreferred (or rare) codons for ∼2-4% of the predicted protein coding genes in both species. The majority (∼74-85%) of these genes are related to pathways involved with translation, energy metabolism and carbohydrate metabolism. Our results suggest that these genes and the related pathways may be under translational selection in these mosquitoes.

Figure 1

Cluster patterns of tRNA genes in both genomes. A) Val-tRNAs in An. gambiae, B) Pro-tRNA genes in An. gambiae. C). Met-tRNA genes in Ae. aegypti. D). Tyr-tRNA genes in An. gambiae. E) Tyr-tRNA genes in Ae. aegypti. The chromosome/supercontig location, along with start and end coordinates, of each cluster is indicated. The numbers on the right side of each cluster indicates the distance between neighboring tRNA genes.

Figure 2

Sequence variation within tRNA genes. The tRNA genes of both species show varying levels of average nucleotide differences. Note that tRNA genes analyzed here are all intron-less copies. The tRNA-Tyr genes are not included in this analysis as each of these genes contains an intron in both species.

Figure 3

Phylogenetic (neighbor-joining tree) relationships of Tyr-tRNA genes of Ae. aegypti (shown as gene IDs starting AAELs) and An. gambiae (shown as gene IDs starting AGAPs). The scale is shown by the vertical line.

Figure 4

Neighbor-joining phylogenetic tree of actin genes show distinct phylogenetic grouping of genes that predominantly show RAIT-dependent codon usage (in bold branching). The genes that show RAIT-dependent codon usage are labeled RAIT after the gene ID.