Abstract
The sea cucumber Apostichopus japonicus is a foodstuff with very high economic value in China, Japan and other countries in south-east Asia. It is at the heart of a multibillion-dollar industry and to meet demand for this product, aquaculture methods and facilities have been established. However, there are challenges associated with optimization of reproduction, feeding and growth in non-natural environments. Therefore, we need to learn more about the biology of A. japonicus, including processes such as aestivation, evisceration, regeneration and albinism. One of the major classes of molecules that regulate physiology and behaviour in animals are neuropeptides, and a few bioactive peptides have already been identified in A. japonicus. To facilitate more comprehensive investigations of neuropeptide function in A. japonicus, here we have analysed genomic and transcriptomic sequence data and proteomic data to identify neuropeptide precursors and neuropeptides in this species. We identified 44 transcripts encoding neuropeptide precursors or putative neuropeptide precursors, and in some instances neuropeptides derived from these precursors were confirmed by mass spectrometry. Furthermore, analysis of genomic sequence data enabled identification of the location of neuropeptide precursor genes on genomic scaffolds and linkage groups (chromosomes) and determination of gene structure. Many of the precursors identified contain homologs of neuropeptides that have been identified in other bilaterian animals. Precursors of neuropeptides that have thus far only been identified in echinoderms were identified, including L- and F-type SALMFamides, AN peptides and others. Precursors of several peptides that act as modulators of neuromuscular activity in A. japonicus were also identified. The discovery of a large repertoire of neuropeptide precursors and neuropeptides provides a basis for experimental studies that investigate the physiological roles of neuropeptide signaling systems in A. japonicus. Looking ahead, some of these neuropeptides may have effects that could be harnessed to enable improvements in the aquaculture of this economically important species.
Highlights
The use of sea cucumbers as a foodstuff, known as trepang or haishen, has been a feature of Chinese culinary culture for hundreds of years[1]
By analyzing novel A. japonicus circumoral nerve ring (CNR) transcriptome sequence data in combination with other publicly available A. japonicus transcriptome sequence data, we have identified 44 candidate neuropeptide precursors
For the purposes of discussion we have divided these into four groups: (1) Precursors of neuropeptides belonging to known bilaterian neuropeptide families (Figs. 1–3), (2) Precursors of neuropeptides belonging to neuropeptide families that have far only been identified in echinoderms and precursors of other putative echinoderm neuropeptides (Figs. 4–5), (3) Precursors of neuropeptides that have been identified as myoactive neuropeptides in A. japonicus (Fig. 6), and (4) Other novel putative neuropeptide precursors identified in A. japonicus based on their sequence similarity with known A. japonicus precursor proteins (Fig. 7)
Summary
The use of sea cucumbers (class Holothuroidea; phylum Echinodermata) as a foodstuff, known as trepang or haishen, has been a feature of Chinese culinary culture for hundreds of years[1]. There is a need to develop better methods for induction of spawning and to improve the growth and quality of the edible body wall tissue of sea cucumbers produced in aquaculture facilities[3]. To accomplish this we need to learn more about the biology of these animals, including genetics, neurophysiology, ecophysiology, www.nature.com/scientificreports/. Stichopin, a 17-amino acid peptide with a disulphide bridge[23], suppresses the stiffening effect of acetylcholine (ACh) on the body wall dermis[27] This effect is consistent with the pattern of expression of stichopin in A. japonicus[28]. With the development of sequencing technologies, further insights into the diversity of neuropeptide precursors in A. japonicus and other sea cucumber species have been obtained recently[33,34]
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