Transcriptome analysis provides insights into the molecular mechanisms responsible for evisceration behavior in the sea cucumber Apostichopus japonicus

The sea cucumber Apostichopus japonicus (Selenka) is a valuable economic species in Southeast Asia. It has many fascinating behavioral characteristics, such as autolysis, aestivation, regeneration, and evisceration, thus it is a notable species for studies of special behaviors. Evisceration and autotomy are controlled by the neural network and involve a complicated physiological process. The occurrence of evisceration behavior in sea cucumbers is strongly related to their environment, and it negatively impacts their economic value. Evisceration behavior plays a pivotal role in the survival of A. japonicas, and when it is induced by dramatic changes in the coastal ecological environment and the aquaculture setting it can strongly affect the economic performance of this species. Although numerous studies have focused on intestinal regeneration of A. japonicas, less is known about evisceration behavior, especially its underlying molecular mechanisms. Thus, identification of genes that regulate evisceration in the sea cucumber likely will provide a scientific explanation for this significant specific behavior. In this study, Illumina sequencing (RNA-Seq) was performed on A. japonicas specimens in three states: normal (TCQ), eviscerating (TCZ), and 3 h after evisceration (TCH). In total, 129,905 unigenes were generated with an N50 length of 2651 base pairs, and 54,787 unigenes were annotated from seven functional databases (KEGG, KOG, GO, NR, NT, Interpro, and Swiss-Prot). Additionally, 190, 191, and 320 genes were identified as differentially expressed genes (DEGs) in the comparisons of TCQ vs. TCZ, TCZ vs. TCH, and TCQ vs. TCH, respectively. These DEGs mapped to 157, 113, and 190 signaling pathways in the KEGG database, respectively. KEGG analyses also revealed that potential DEGs enriched in the categories of "environmental information processing," "organismal system," "metabolism," and "cellular processes," and they were involved in evisceration behavior in A. japonicas. These DEGs are related to muscle contraction, hormone and neurotransmitter secretion, nerve and muscle damage, energy support, cellular stress, and apoptosis. In conclusion, through our comparative analysis of A. japonicus in different stages, we identified many candidate evisceration-related genes and signaling pathways that likely are involved in evisceration behavior. These results should help further elucidate the mechanisms underlying evisceration behavior in sea cucumbers.