Evolution of the tRNA gene family in mitochondrial genomes of five Meretrix clams (Bivalvia, Veneridae)

• Mitochondrial genome of Meretrix lyrata was characterized.
• Duplication of trnM in different bivalve lineages may have occurred more recently.
• Horizontal evolution is important in bivalves’ tRNA gene family evolution.
• The first case of isoacceptor VTGR in mollusk was reported.
• Vertical tRNA gene recruitment in mollusk allows rapid evolution of tRNAs.

In contrast to the extreme conservation of nuclear-encoded tRNAs, organization of the mitochondrial (mt) tRNA gene family in invertebrates is highly dynamic and rapidly evolving. While gene duplication and loss, gene isomerism, recruitment, and rearrangements have occurred sporadically in several invertebrate lineages, little is known regarding the pattern of their evolution. Comparisons of invertebrate mt genomes at a generic level can be extremely helpful in investigating evolutionary patterns of variation, as intermediate stages of the process may be identified. Variation of mitochondrial tRNA organization among Meretrix clams provides good materials to investigate mt tRNA evolution. We characterized the complete mt genome of the lyrate Asiatic hard clam Meretrix lyrata, re-annotated tRNAs of four previously sequenced Meretrix clams, and undertook an intensive comparison of tRNA gene families in these clams. Our results 1) provide evidence that the commonly observed duplication of trnM may have occurred independently in different bivalve lineages and, based on the higher degree of trnM gene similarity, may have occurred more recently than expected; 2) suggest that “horizontal” evolution may have played an important role in tRNA gene family evolution based on frequent gene duplications and gene recruitment events; and 3) reveal the first case of isoacceptor “vertical” tRNA gene recruitment (VTGR) and present the first clear evidence that VTGR allows rapid evolution of tRNAs. We identify the trnS− UCR gene in Meretrix clams, previously considered missing in this lineage, and speculate that trnS− UCR lacking the D-arm in both M. lyrata and Meretrix lamarckii may represent the ancestral status. Phylogenetic analysis based on 13 concatenate protein-coding genes provided opportunities to detect rapidly evolved tRNA genes via VTGR and gene isomerism processes. This study suggests that evolution of the mt tRNA gene family in bivalves is more complex than previously thought and that comparison of several congeneric species is a useful strategy in investigating evolutionary patterns and dynamics of mt tRNA genes.