Research Article: The complete mitochondrial genome of Calyptogena marissinica (Heterodonta: Veneroida: Vesicomyidae): Insight into the deep-sea adaptive evolution of vesicomyids

Date Published: September 19, 2019

Publisher: Public Library of Science

Author(s): Mei Yang, Lin Gong, Jixing Sui, Xinzheng Li, Marc Robinson-Rechavi.

http://doi.org/10.1371/journal.pone.0217952

Abstract

The deep-sea chemosynthetic environment is one of the most extreme environments on the Earth, with low oxygen, high hydrostatic pressure and high levels of toxic substances. Species of the family Vesicomyidae are among the dominant chemosymbiotic bivalves found in this harsh habitat. Mitochondria play a vital role in oxygen usage and energy metabolism; thus, they may be under selection during the adaptive evolution of deep-sea vesicomyids. In this study, the mitochondrial genome (mitogenome) of the vesicomyid bivalve Calyptogena marissinica was sequenced with Illumina sequencing. The mitogenome of C. marissinica is 17,374 bp in length and contains 13 protein-coding genes, 2 ribosomal RNA genes (rrnS and rrnL) and 22 transfer RNA genes. All of these genes are encoded on the heavy strand. Some special elements, such as tandem repeat sequences, “G(A)nT” motifs and AT-rich sequences, were observed in the control region of the C. marissinica mitogenome, which is involved in the regulation of replication and transcription of the mitogenome and may be helpful in adjusting the mitochondrial energy metabolism of organisms to adapt to the deep-sea chemosynthetic environment. The gene arrangement of protein-coding genes was identical to that of other sequenced vesicomyids. Phylogenetic analyses clustered C. marissinica with previously reported vesicomyid bivalves with high support values. Positive selection analysis revealed evidence of adaptive change in the mitogenome of Vesicomyidae. Ten potentially important adaptive residues were identified, which were located in cox1, cox3, cob, nad2, nad4 and nad5. Overall, this study sheds light on the mitogenomic adaptation of vesicomyid bivalves that inhabit the deep-sea chemosynthetic environment.

Partial Text

Mitochondria, which descended from Proteobacteria via endosymbiosis, are important organelles in eukaryotic cells and are involved in various processes, such as ATP generation, signaling, cell differentiation, growth and apoptosis [1]. Moreover, mitochondria have their own genetic information system. In general, the metazoan mitogenome is a closed, circular DNA molecule, ranging from 12 to 20 kb in length and usually containing 37 genes: 13 protein-coding genes (PCGs) (atp6, atp8, cox1-3, cob, nad1-6 and nad4l) of the respiratory chain, 2 ribosomal RNA (rRNA) genes (rrnS and rrnL) and 22 transfer RNA (tRNA) genes [2]. In addition, there are several noncoding regions in the mitogenome, and the longest noncoding “AT-rich” region is normally interpreted as the control region (CR), which includes elements controlling the initiation and regulation of transcription and replication [3]. Owing to variable gene order, a low frequency of gene recombination and different genes having different evolutionary rates, mitochondrial sequences are widely used for species identification, genetic diversity assessment and phylogenetics at various taxonomic levels [4–7].

This study characterized the complete mitogenome of the deep-sea vesicomyid bivalve C. marissinica, which is 17,374 bp in length and encodes 37 typical mitochondrial genes, including 13 PCGs, 2 rRNA genes, and 22 tRNA genes. All of these genes are encoded on the heavy strand. We analyzed the mitogenome organization, codon usage, control region features, gene arrangement, phylogenetic relationships and positive selection of C. marissinica. In the mitogenome of C. marissinica, tandem repeat sequences, “G(A)nT” motifs and AT-rich sequences were detected. In the family Vesicomyidae, we found that if the tRNA genes are not considered, the sequenced vesicomyid bivalves have a completely identical arrangement of PCGs. The phylogenetic analyses clustered C. marissinica with previously reported vesicomyid bivalves with high support values. Ten residues located in cox1, cox3, cob, nad2, nad4 and nad5 were inferred to be positively selected sites along the branches leading to vesicomyid bivalves, which may indicate that the genes were under positive selection pressure. The findings of this study could help deepen our understanding of the molecular mechanisms of adaptive evolution at the mitochondrial level in deep-sea organisms.

 

Source:

http://doi.org/10.1371/journal.pone.0217952

 

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