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.

Author summary

Echinoderms, ubiquitous in the marine environment, are important from evolutionary, ecological, and socioeconomic perspectives. Together with chordates and hemichordates, they form the deuterostome clade, making them a crucial node in the study of chordate ancestry. Within echinoderms, class Holothuroidea is unique; its members (the sea cucumbers) display remarkable regenerative abilities and play key roles as sediment bioturbators and symbiotic hosts, and many are prized in the seafood and pharmaceutical industries. The sea cucumber genome therefore has the potential to significantly contribute to our understanding of important evolutionary and biological processes and help enhance aquaculture programs. Here we present a high-quality genome sequence for the economically important species Apostichopus japonicus. Through comparative analyses, we identified 763 echinoderm-specific gene families enriched in genes encoding membrane proteins, ion channels, and signal transduction proteins. Marker genes associated with the notochord and gill slits were also found, providing valuable insight into the origin of chordates. The reduced number and low expression levels of biomineralization genes reflect the skeletal degeneration seen in sea cucumbers. Importantly, 2 gene families appeared to be expanded in A. japonicus and may play crucial roles in its heightened regenerative potential. Together, findings from the sea cucumber genome provide important and novel insights into echinoderm and deuterostome biology.