The C-Terminal Extension That Characterizes Mosquito (Diptera: Culicidae) Ribosomal Protein S6 Is Widespread Among the Culicomorpha

Abstract

Eukaryotic ribosomal proteins, which participate in the structure and function of the translational machinery, are generally well conserved. In Aedes and Anopheles mosquitoes (Diptera: Culicidae), however, ribosomal protein S6 (RpS6) contains a low-complexity, C-terminal extension that is absent from its homolog in Drosophila melanogaster Meigen and Manduca sexta (L.). To explore the distribution of RpS6 C-terminal extensions in genera phylogenetically closer to mosquitoes than is Drosophila, we recovered cDNAs encoding RpS6 from a phantom midge (Chaoborus sp.), a midge (Chironomus sp.), a blackfly (Simulium sp.), and a phantom crane fly [Bittacomorpha clavipes (F.)]. Sequences of deduced translation products showed that RpS6 extensions occurred only in members of the Culicomorpha, and they were absent from B. clavipes, a member of the Ptychopteromorpha, which forms the sister group to the Culicomorpha. Likewise, the extension did not occur in Telamtoscopus sp., a moth fly classified among the more distantly related Psychodomorpha. The C-terminal extensions on RpS6 ranged in length from 81 to 190 amino acids, they were highly enriched for lysine and alanine, and they seem to be evolving more rapidly than the conventional portion of the RpS6 protein shared by all eukaryotes. Although analysis of RpS6 protein was consistent with analyses based on ribosomal DNA, suggesting that Chironomidae is the sister group to the remaining families in the Culicomorpha, trees generated from RpS6 amino acid sequences were largely congruent with accepted phylogenies based on morphological characters. Our results suggest that a C-terminal, lysine-rich extension on RpS6 is a potential molecular synapomorphy for the Culicomorpha.