Comparative mitochondrial genomic analyses of three chemosynthetic vesicomyid clams from deep-sea habitats

Abstract

Vesicomyid clams of the subfamily Pliocardinae are among the dominant chemosymbiotic bivalves found in sulfide-rich deep-sea habitats. Plastic morphologies and present molecular data could not resolve taxonomic uncertainties. The complete mitochondrial (mt) genomes will provide more data for comparative studies on molecular phylogeny and systematics of this taxonomically uncertain group, and help to clarify generic classifications. In this study, we analyze the features and evolutionary dynamics of mt genomes from three Archivesica species (Archivesica sp., Ar. gigas and Ar. pacifica) pertaining to subfamily Pliocardinae. Sequence coverage is nearly complete for the three newly sequenced mt genomes, with only the control region and some tRNA genes missing. Gene content, base composition, and codon usage are highly conserved in these pliocardiin species. Comparative analysis revealed the vesicomyid have a relatively lower ratio of Ka/Ks, and all 13 protein-coding genes (PGCs) are under strong purifying selection with a ratio of Ka/Ks far lower than one. Minimal changes in gene arrangement among vesicomyid species are due to the translocation trnaG in Isorropodon fossajaponicum. Additional tRNA genes were detected between trnaG and nad2 in Abyssogena mariana (trnaL3), Ab. phaseoliformis (trnaS3), and Phreagena okutanii (trnaM2), and display high similarity to other pliocardiin sequences at the same location. Single base insertion in multiple sites of this location could result in new tRNA genes, suggesting a possible tRNA arising from nongeneic sequence. Phylogenetic analysis based on 12 PCGs (excluding atp8) supports the monophyly of Pliocardiinae. These nearly complete mitogenomes provide relevant data for further comparative studies on molecular phylogeny and systematics of this taxonomically uncertain group of chemosymbiotic bivalves.

Keywords: chemosymbiotic bivalves; deep‐sea; gene arrangement; mitochondrial genome; vesicomyid clams.

Figure 1

Compositional patterns of Archivesica sp., Ar. gigas, and Ar. pacifica mitochondrial genomes. AT content, A − T skew, and G − C skew are computed for each protein‐coding genes (PCGs) and rRNAs, and for PCGs, rRNA and tRNAs taken as a whole

Figure 2

Evaluation of codon bias in the mitochondrial genomes of eight vesicomyid species. ENC, effective number of codons; CBI, codon bias index; G + Cc, G + C content of all codon positions; G + C3s, G + C content of the third codon positions

Figure 3

Comparison of sequence divergence for each mitochondrial gene. Vesicomyid clams including eight species. The genus Paphia includes P. textile, P. undulata, P. amabilis, and P. euglypta. The genus Meretrix includes M. petechialis, M. lusoria, M. lamarckii, and M. lyrata

Figure 4

Gene rearrangements. Reconstruction of relationships among gene arrangements of vesicomyid, Meretrix lyrata, Arctica islandica is shown, after the exclusion of tRNAs. Atp8* missed in bivalve A. islandica

Figure 5

Gene order of mt genomes from eight vesicomyid clams. All species with complete or nearly complete mt genomes are listed. Noncoding region means none coding region. White colors indicate changes compared to the “C.” magnifica pattern. Asterisks indicate genes insertion and underlines refer to gene translocation event

Figure 6

Alignment of sequence located between trnaG and nad2 in eight vesicomyid mt genomes (a), and tRNA detection in the putative sequence based on “Calyptogena” magnifica mt genome after base insertion (b)

Figure 7

Phylogenetic relationship of Heterodonta based on the concatenated nucleotide sequences of 12 mt protein‐coding genes. Numbers on branches are bootstrap probability of Neighbor‐joining method (left) and Maximum‐likelihood method (right). Two Ostreidae species belong to the subclass Pteriomorphia are used to root the tree. Red type face indicates the species for which mt genomes are determined in the present study