The Evolutionary Dynamics of the Mitochondrial tRNA in the Cichlid Fish Family

Simple Summary Cichlids are a unique example of fish diversity and species richness which have been explained by sympatric speciation at different freshwater sources in Africa. The mitochondria contribute to cell vitality by providing energy. It contains a circular genome with an established translation system that is spatially independent of the cytosolic counterpart. The current study aimed to investigate the evolutionary dynamics of the mitochondrial tRNA and its role in cichlids' diversity. The available cichlid mitogenomes in the public database were filtered, in addition to newly sequenced accessions from a specific cichlid group known as the haplotilapiine lineage that is widely distributed in the Egyptian sector of the Nile River. Based on the comparative analysis of mitogenomic data, we identified 22 tRNA genes, in which a single gene was D-armless, while the cloverleaf secondary structure subdivided into stem-loop formations was predicted and used to define the levels of genetic divergence for the remained tRNAs. Peculiarly, in cichlids, the formation known as T-arm showed the lowest polymorphism levels among other structures in contrast to other organisms (e.g., scorpions). Comparing the whole family to the specific haplotilapiine lineage showed that the tryptophan tRNA was the most conserved tRNA, with signatures of possible purifying selection. The mitochondrial transfer RNA genes (tRNAs) attract more attention due to their highly dynamic and rapidly evolving nature. The current study aimed to detect and evaluate the dynamics, characteristic patterns, and variations of mitochondrial tRNAs. The study was conducted in two main parts: first, the published mitogenomic sequences of cichlids mt tRNAs have been filtered. Second, the filtered mitochondrial tRNA and additional new mitogenomes representing the most prevalent Egyptian tilapiine were compared and analyzed. Our results revealed that all 22 tRNAs of cichlids folded into a classical cloverleaf secondary structure with four domains, except for trnS(GCU), missing the D domain in all cichlids. When consensus tRNAs were compared, most of the mutations were observed in the trnP at nucleotide levels (substitutions and indels), in contrast to trnL(UAA). From a structural perspective, the anticodon loop and T-loop formations were the most conserved structures among all parts of the tRNA in contrast to the A-stem and D-loop formations. The trnW was the lowest polymorphic unneutral tRNA among all cichlids (both the family and the haplotilapiine lineage), in contrast with the neutral trnD that was extremely polymorphic among and within the haplotilapiine lineage species compared to other cichlids species. From a phylogenetic perspective, the trnC was extremely hypervariable and neutral tRNA in both haplotilapiine lineage and cichlids but was unable to report correct phylogenetic signal for the cichlids. In contrast to trnI and trnY, less variable neutral tRNAs that were able to cluster the haplotilapiine lineage and cichlids species as previously reported. By observing the DNA polymorphism in the coding DNA sequences (CDS), the highest affected amino acid by non-synonymous mutations was isoleucine and was equally mutated to valine and vice versa; no correlation between mutations in CDS and tRNAs was statistically found. The current study provides an insight into the mitochondrial tRNA evolution and its effect on the cichlid diversity and speciation model at the maternal level.

Automated summary

This study focuses on the evolutionary dynamics of mitochondrial tRNA in cichlids and its impact on cichlid diversity. Comparative analysis of mitogenomic data reveals varying levels of genetic divergence in different tRNA structures in cichlids.