Comparative mitogenomics of Clupeoid fish provides insights into the adaptive evolution of mitochondrial oxidative phosphorylation (OXPHOS) genes and codon usage in the heterogeneous habitats

Clupeoid fish can be considered excellent candidates to understand the role of mitochondrial DNA in adaptive evolution, as they have colonized different habitats (marine, brackish, freshwater, tropical and temperate regions) over millions of years. Here, we investigate patterns of tRNA location, cod...

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Bibliographic Details
Published in:Heredity 2022-04, Vol.128 (4), p.236-249
Main Authors: Sebastian, Wilson, Sukumaran, Sandhya, Gopalakrishnan, A
Format: Article
Language:English
Subjects:
Amino acids
Amino Acids - genetics
Animals
Aquatic habitats
Codon - genetics
Codon Usage
Codons
Complementarity
Deamination
DNA, Mitochondrial - genetics
Ecosystem
Efficiency
Evolution
Evolution & development
Evolution, Molecular
Evolutionary genetics
Fish
Fishes - genetics
Genes
Genes, Mitochondrial
Habitats
Metabolism
Mitochondrial DNA
Oxidative Phosphorylation
Phosphorylation
Pressure
RNA, Transfer - genetics
Selection, Genetic
Transcription
Transfer RNA
Translation
tRNA
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Summary:Clupeoid fish can be considered excellent candidates to understand the role of mitochondrial DNA in adaptive evolution, as they have colonized different habitats (marine, brackish, freshwater, tropical and temperate regions) over millions of years. Here, we investigate patterns of tRNA location, codon usage bias, and lineage-specific diversifying selection signals to provide novel insights into how evolutionary improvements of mitochondrial metabolic efficiency have allowed clupeids to adapt to different habitats. Based on whole mitogenome data of 70 Clupeoids with a global distribution we find that purifying selection was the dominant force acting and that the mutational deamination pressure in mtDNA was stronger than the codon/amino acid constraints. The codon usage pattern appears evolved to achieve high translational efficiency (codon/amino acid-related constraints), as indicated by the complementarity of most codons to the GT-saturated tRNA anticodon sites (retained by deamination-induced pressure) and usage of the codons of the tRNA genes situated near to the control region (fixed by deamination pressure) where transcription efficiency was high. The observed shift in codon preference patterns between marine and euryhaline/freshwater Clupeoids indicates possible selection for improved translational efficiency in mitochondrial genes while adapting to low-salinity habitats. This mitogenomic plasticity and enhanced efficiency of the metabolic machinery may have contributed to the evolutionary success and abundance of Clupeoid fish.
ISSN:0018-067X
1365-2540
DOI:10.1038/s41437-022-00519-z