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

Abstract

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.

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Fig. 1: Geographical distribution pattern of the Clupeoids.
Fig. 2: Maximum likelihood phylogenetic tree generated out of complete mitogenome nucleotide sequences of Clupeoids.
Fig. 3: Nucleotide composition of genes in Clupeoid mitogenome and order of distribution of tRNA along H and L strand.
Fig. 4: Heat map of nucleotide composition at different codon positions of merged protein-coding genes of Clupeoid fish.
Fig. 5: Candidate sites for selection in Cytochrome C Oxidase (Complex IV).
Fig. 6: Radical physicochemical amino acid changes associated with divergence of mitogenome of Clupeoids.

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All DNA sequences used in this study are from the publically available database, GenBank and accession numbers are included in the manuscript Supplementary file_1_Table S4.

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Acknowledgements

We would like to thank the Director, Central Marine Fisheries Research Institute (CMFRI) and Dr P. Vijayagopal (Head, Marine Biotechnology Division, ICAR-CMFRI) for providing facilities to carry out this work. WS received a Senior Research Fellowship from the ICAR-NICRA project. This work was carried out under the institute project MBT/GEN/25, receiving funding support from the Indian Council of Agricultural Research (ICAR).

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WS conceived the idea, conducted the research, interpreted the results, and wrote the first manuscript. SS coordinated the research, interpreted the results and wrote the first manuscript. AG reviewed the original manuscript, provided feedback and approved it.

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Correspondence to Sandhya Sukumaran.

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The authors declare no competing interests.

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Associate editor: Bastiaan Star.

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Sebastian, W., Sukumaran, S. & Gopalakrishnan, A. Comparative mitogenomics of Clupeoid fish provides insights into the adaptive evolution of mitochondrial oxidative phosphorylation (OXPHOS) genes and codon usage in the heterogeneous habitats. Heredity 128, 236–249 (2022). https://doi.org/10.1038/s41437-022-00519-z

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