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

Xiaojun Zhang,Shilin Liu,Yang Yu,Shihao Li,Fuhua Li,Lei Wang,Yi Zhou,Jianhai Xiang,Lina Sun,Hongsheng Yang,Yi Gao,Jianbo Yuan,Xiaoni Li,Da Huo,Peng Xu,Lili Xing,Wenchao Lin,Kenneth B Storey,Hui Dai,Yamin Sun,Pin Huan,Kaimin Guo,Tao Zhang,Annie Mercier,Libin Zhang,Mingzhe Sun,Jiquan Zhang,Chenggang Lin,Jean‐François Hamel ,Xianhui Qin ,Shiwei Jin

doi:10.1371/journal.pbio.2003790

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.

Highlights

IntroductionEchinodermata, an ancient phylum of marine invertebrates, comprises 5 extant classes, including Echinoidea (sea urchins), Asteroidea (sea stars), Holothuroidea (sea cucumbers), Ophiuroidea (brittle stars), and Crinoidea (sea lilies)
Echinodermata, an ancient phylum of marine invertebrates, comprises 5 extant classes, including Echinoidea, Asteroidea, Holothuroidea, Ophiuroidea, and Crinoidea
The genome of A. japonicus was sequenced using a combination of Illumina shot-gun and PacBio Single Molecule Real-Time (SMRT) sequencing

Summary

Introduction

Echinodermata, an ancient phylum of marine invertebrates, comprises 5 extant classes, including Echinoidea (sea urchins), Asteroidea (sea stars), Holothuroidea (sea cucumbers), Ophiuroidea (brittle stars), and Crinoidea (sea lilies). 2 complete echinoderm genomes, that of the sea urchin Strongylocentrotus purpuratus and that of the sea star Acanthaster planci, have been successfully sequenced [1,2]. Because sea cucumbers are unique among echinoderms, possessing many distinctive biological characteristics, their genome holds invaluable insight that can extend the scope and depth of molecular research in Echinodermata and Deuterostomia. Sea cucumber adults exhibit an elongated shape that belies their pentaradial symmetry, combined with weak calcification in the form of microscopic ossicles that contrasts with the solid calcified test of sea urchins. Exploring these features can help in exploring the evolution of mineralization in echinoderms, which remains poorly understood

Methods

Results

Conclusion