Codon Usage Evolution in Opisthokonta

The emergence of life on Earth developed a system of DNA containing the information inherited in the reproduction of organisms, directing also the variability of life as this changes. The language using for deciphering the DNA is the genetic code, which is degenerated as 20 amino acids are codified by 64 codons, or triplets of nitrogenous bases (adenine, guanine, cytosine and thymine) in the nucleotides that form the DNA. 59 codons have other/s synonymous codons, and those are not used randomly but are a product of different phenomena. The drivers of codon usage bias can be mutations, genetic drift and natural selection processes. The study of these codons can provide evolutionary information, like gene family evolution and organisation, can offer an insight in population size, and also can be used to create software to predict ORFs and coding regions. Codon study also can be important in biotechnology for heterologous expression, as the codon used have a control over the efficiency and accuracy during translation, resulting in determinant for protein folding, growth rate and avoidance of defective proteins.

Opisthokonta is a group of organisms, close to Apusomonadida, and gathering Holozoa (Ichthyosporea, Filasterea, Choanoflagellatea and Metazoa) and Holomycota. The present study uses the transcriptome of 20 choanoflagellates species, Sphaeroforma arctica (Class Ichthyosporea), Thecamonas trahens (class Apusomonadea) and five early branching metazoans (Amphimedon queenslandica, Mnemiopsis leidyi, Nematostella vectensis, Thelohanellus kitauei and Trichoplax adhaerens) to study the codon usage bias and anticodon related phenomena in the mentioned species.

Analysis revealed optimal codons for each organism, with a GC ended codons enrichment in T. trahens, unicellular Opisthokonta, and retained after the transition to pluricellularity (with divergences in M. leidyi and N. vectensis). All the unicellular species showed evidence for natural selection upon translational accuracy and efficiency, even the less biased ones. In metazoan only translational efficiency was evidenced, with lower strength of selection, and poor support for translational accuracy in ctenophoran and cnidarian species. For other strategies giving advantages on protein translation, indirect evidence of deamination in high degenerated amino acids was found in all the species studied, while direct evidence was found in S. arctica, A. queenslandica, M. leidyi and N. vectensis. Additionally, tRNA presenting isotype-anticodon disagreements were found in apusomonadean, ichthyosporean, metazoan species and in S. rosetta. Deamination, and possibly chimeric tRNA appeared early in evolution, before the divergence of Apusomonadea and Opisthokonta, benefiting the use of optimal codons through evolution until the apparition of the latest metazoan organisms.