The sea cucumber genome provides insights into morphological evolution and visceral regeneration

Abstract

Apart from sharing common ancestry with chordates, sea cucumbers exhibit a unique morphology and exceptional regenerative capacity. Here we present the complete genome sequence of an economically important sea cucumber, A. japonicus, generated using Illumina and PacBio platforms, to achieve an assembly of approximately 805 Mb (contig N50 of 190 Kb and scaffold N50 of 486 Kb), with 30,350 protein-coding genes and high continuity. We used this resource to explore key genetic mechanisms behind the unique biological characters of sea cucumbers. Phylogenetic and comparative genomic analyses revealed the presence of marker genes associated with notochord and gill slits, suggesting that these chordate features were present in ancestral echinoderms. The unique shape and weak mineralization of the sea cucumber adult body were also preliminarily explained by the contraction of biomineralization genes. Genome, transcriptome, and proteome analyses of organ regrowth after induced evisceration provided insight into the molecular underpinnings of visceral regeneration, including a specific tandem-duplicated prostatic secretory protein of 94 amino acids (PSP94)-like gene family and a significantly expanded fibrinogen-related protein (FREP) gene family. This high-quality genome resource will provide a useful framework for future research into biological processes and evolution in deuterostomes, including remarkable regenerative abilities that could have medical applications. Moreover, the multiomics data will be of prime value for commercial sea cucumber breeding programs.

Genome-wide comparative analysis of theSHSP,HSP60/10andHSP90genes reveals differential heat stress responses in estivation of the sea cucumberApostichopus japonicus

“…Interestingly, in some cases, the SHSPs of the acorn worm grouped with the counterparts of echinoderms. This finding is consistent with the conclusion of Zhang et al, which suggested that echinoderms and hemichordates were sister groups and shared a common ancestor (Zhang et al, ).…”

“…The Latin name of each species is listed in Appendix: Supplementary Table S3. hemichordates were sister groups and shared a common ancestor (Zhang et al, 2017).…”

“…The sea cucumber SHSP , HSP60/10 and HSP90 genes were identified by searching against 10 RNA‐seq databases (GFKU01, HADE01, GAVS01, GFLK01, GFXQ01, HADF01, HADD01 and three other groups in our unpublished data) and the whole genome sequence database of the sea cucumber (Zhang et al, ). All available SHSP , HSP60/10 and HSP90 genes from vertebrate species were used, from teleosts to mammals (zebrafish ( Danio rerio ), clawed frog ( Xenopus tropicalis ), lizard ( Anolis carolinensis ), mouse ( Mus musculus ) and human ( Homo sapiens )), cephalochordate (amphioxus ( Branchiostoma belcheri )), urochordate (ascidian ( Ciona intestinalis )), hemichordate (acorn worm ( Saccoglossus kowalevskii )), echinoderms (sea urchin ( Strongylocentrotus purpuratus ) and starfish ( Acanthaster planci )), arthropod (fruit fly ( Drosophila melanogaster )) and nematode ( Caenorhabditis elegans ), and query sequences were retrieved from the NCBI (http://www.ncbi.nlm.nih.gov) and Ensembl (http://www.ensembl.org) databases.…”

The polymorphism ofHydramicrosatellite sequences provides strain-specific signatures

“…The c25145 gene encodes a putative evolutionarily-conserved protein with an unknown function as deduced from the alignment of the Hydra c25145 deduced protein product with related bilaterian sequences ( Fig S4 ). We found similarities in the N-terminal moiety (~100 first amino acids) with hypothetical proteins expressed by the sea cucumber Apostichopus japonicus (51), the arthropods Folsomia candida and Sipha flava (aphid), the mollusc Crassostrea gigas , the teleost fish Myripristis murdjan, Sinocyclocheilus rhinocerous or Danio rerio . Within this domain, a signature can be identified, formed of 37 residues, from which 32 are present in the Hydra protein ( Fig S4 ).…”

A preliminary identification of genomic loci for body colour variation in the sea cucumberApostichopus japonicus

“…However, only one QTL for growth was reported (Tian et al, ) and none GWAS has been conducted in sea cucumber A. japonicus . Recently, the whole genome sequences of A. japonicus have been published and a database was established (Zhang et al, ), which will carry forward QTL analysis and candidate gene identification in sea cucumber A. japonicus .…”