The first two complete mitogenomes of the order Apodida from deep-sea chemoautotrophic environments: New insights into the gene rearrangement, origin and evolution of the deep-sea sea cucumbers.

The deep-sea ecosystem is considered as the largest and most remote biome of the world. It is meaningful and important to elucidate the life origins by exploring the origin and adaptive genetic mechanisms of the large deep-sea organisms. Sea cucumbers (Holothuroidea) are abundant and economically important group of echinoderms, living from the shallow-waters to deep-sea. In this study, we present the mitochondrial genomes of the sea cucumber Chiridota heheva and Chiridota sp. collected from the deep-sea cold seep and hydrothermal vent, respectively. This is the first reported mitochondrial genomes from the order Apodida. The mitochondrial genomes of C. heheva (17,200 bp) and Chiridota sp. (17,199 bp) display novel gene arrangements with the first protein-coding gene rearrangements in the class Holothuroidea. Bases composition analysis showed that the A + T content of deep-sea holothurians were significantly higher than that of the shallow-water groups. We compared the arrangement of genes from the 24 available holothurian mitogenomes and found that the transposition, reverse transposition and tandem-duplication-random-losses (TDRL) may be involved in the evolution of mitochondrial gene arrangements in Holothuroidea. Phylogenetic analysis revealed that the Apodida clustered with Elasipodida, forming two basal deep-sea holothurian clades. The divergence between the deep-sea and shallow-water holothurians was located at 386.93 Mya, during the Late Devonian. Mitochondrial protein-coding genes of deep-sea holothurians underwent relaxed purifying selection. There are 57 positive selected amino acids sites for some mitochondrial genes of the three deep-sea clades, implying they may involve in the adaption of deep-sea sea cucumbers.