The complete mitochondrial genome ofCalyptogena marissinica(Heterodonta: Veneroida: Vesicomyidae): insight into the deep-sea adaptive evolution of vesicomyids

Abstract

12The deep sea is one of the most extreme environments on earth, with low oxygen, high hydrostatic 13 pressure and high levels of toxins. Species of the family Vesicomyidae are among the dominant 14 chemosymbiotic bivalves found in this harsh habitat. Mitochondria play a vital role in oxygen usage 15 and energy metabolism; thus, they may be under selection during the adaptive evolution of deep-sea 16 vesicomyids. In this study, the mitochondrial genome (mitogenome) of the vesicomyid bivalve 17 Calyptogena marissinica was sequenced with Illumina sequencing. The mitogenome of C. marissinica 18 is 17,374 bp in length and contains 13 protein-coding genes, 2 ribosomal RNA genes (rrnS and rrnL) 19 and 22 transfer RNA genes. All of these genes are encoded on the heavy strand. Some special elements, 20 such as tandem repeat sequences, "G(A) n T" motifs and AT-rich sequences, were observed in the 21 control region of the C. marissinica mitogenome, which is involved in the regulation of replication and 22 transcription of the mitogenome and may be helpful in adjusting the mitochondrial energy metabolism 23 of organisms to adapt to the deep-sea environment. The gene arrangement of protein-coding genes was 24 identical to that of other sequenced vesicomyids. Phylogenetic analyses clustered C. marissinica with 25 previously reported vesicomyid bivalves with high support values. Positive selection analysis revealed 26 evidence of adaptive change in the mitogenome of Vesicomyidae. Ten potentially important adaptive 27 residues were identified, which were located in cox1, cox3, cob, nad2, nad4 and nad5. Overall, this 28 study sheds light on the mitogenomic adaptation of vesicomyid bivalves that inhabit the deep-sea 29 environment. 2 30 Introduction 31 Mitochondria, which descended from proteobacteria via endosymbiosis, are important organelles in 32 eukaryotic cells and are involved in various processes, such as ATP generation, signaling, cell 33 differentiation, growth and apoptosis [1]. Moreover, mitochondria have their own genetic information 34 system. In general, the metazoan mitogenome is a closed, circular DNA molecule, ranging from 12 to 35 20 kb in length and usually containing 37 genes: 13 protein-coding genes (PCGs) (atp6, atp8, cox1-3, 36 cytb, nad1-6 and nad4l) of the respiratory chain, 2 ribosomal RNA (rRNA) genes (rrnS and rrnL) and 37 22 transfer RNA (tRNA) genes [2]. In addition, there are several noncoding regions in the mitogenome, 38 and the longest noncoding "AT-rich" region is known as the control region (CR), which includes 39 elements controlling the initiation and regulation of transcription and replication [3]. Owing to maternal 40 inheritance, variable gene order, a low frequency of gene recombination and different genes having 41 different evolutionary rates, mitochondrial sequences are widely used for species identification, genetic 42 diversity assessment and phylogenetics at various taxonomic levels [4][5][6][7]. 43Since the discovery of cold seeps and hydrothermal vents in the deep sea, the uni...

Phylogenetic Relationships and Adaptation in Deep-Sea Mussels: Insights from Mitochondrial Genomes

“…In addition, the ω values for all PCGs, except for the cox1 gene, in deep-sea mussels were higher than those in sublittoral species, indicating that the mitogenomes of deep-sea mussels underwent a more relaxed purifying selection. Low ω values for mitochondrial PCGs were also reported in other deep-sea animals, including deep-sea vesicomyids [3,21], a giant Bathynomus sp. [40], and deep-sea polynoids [35].…”

“…Although cob is a conserved gene, it is crucial to the ability of the mitochondria to generate energy through reversible electron transfer from ubiquinol to cytochrome c along with proton translocation. cob was shown to have undergone positive selection in deep-sea fish [19] and deep-sea clams [21]. Therefore, mitochondrial genes, particularly atp6, nad4, nad2, cob, nad5, and cox2, may help deep-sea mussels to survive and/or thrive under harsh deep-sea conditions.…”

“…Mitogenomes carry useful evolutionary information and have been widely applied in phylogenetic and evolutionary studies of terrestrial and shallow-water organisms, including mussels [14][15][16][17]. Given that the mitochondria play a key role in the energetic metabolism of metazoans, the hypoxia and high hydrostatic pressure environments in cold seeps and hydrothermal vents could exert selective pressure on the evolution of these energy-producing organelles [18][19][20][21]. However, only six Bathymodiolinae mitogenomes are currently available, thereby hindering our understanding of their evolution.…”

The complete mitogenome of Phymorhynchus sp. (Neogastropoda, Conoidea, Raphitomidae) provides insights into the deep‐sea adaptive evolution of Conoidea

“…Under these harsh conditions, organisms may require modified and adapted energy metabolism, and evidence of adaptive evolution in complex I has been reported in the mitogenomes of deep‐sea alvinocaridid shrimp, vesicomyids, sea anemones ( Bolocera sp. ), and sea cucumbers ( Benthodytes marianensis ) (Mu et al., 2018b; Sun et al., 2018; Yang et al., 2019; Zhang, Wu, et al., 2020; Zhang, Gao, et al., 2020). Complex III contains eleven subunits, one of which is encoded by the mitochondrial cytb gene (Koopman et al., 2013) and catalyzes reversible electron transfer from ubiquinol to cytochrome c coupled to proton translocation (Trumpower, 1990).…”

Ultrastructural aspects of spermatogenesis in Calyptogena pacifica Dall 1891 (Vesicomyidae; Bivalvia)

“…Mollusks of this family often dominate the molluscan fauna at deep‐sea hydrothermal vents and cold seeps (Tyler & Young, 1999). This habitat is characterized by the lack of light and photosynthesis‐derived nutrients, a high hydrostatic pressure, variable temperatures, a low dissolved oxygen, and high concentrations of hydrogen sulfide (H 2 S), methane (CH 4 ), and heavy metals such as iron, copper, and zinc (Tarasov et al, 2005; Yang, Gong, Sui, & Li, 2019). However, the density of mollusks can be high, reaching several hundreds or even a thousand of individuals per square meter (Barry, Whaling, & Kochevar, 2007; Fujikura, Hashimoto, & Okutani, 2002; Hashimoto et al, 1989).…”