Dataset Information

Neuropeptide precursors and neuropeptides in the sea cucumber Apostichopus japonicus: a genomic, transcriptomic and proteomic analysis.

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.

SUBMITTER: Chen M

PROVIDER: S-EPMC6586643 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Neuropeptide precursors and neuropeptides in the sea cucumber Apostichopus japonicus: a genomic, transcriptomic and proteomic analysis.

Chen Muyan M Talarovicova Alzbeta A Zheng Yingqiu Y Storey Kenneth B KB Elphick Maurice R MR

Scientific reports 20190620 1

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 ...[more]

PMID: 31222106

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Project description:Neuropeptides are endogenous active substances that are present in nervous tissues and participate in behavioral and physiological processes of the animal system. Locomotor behavior is basic to predation, escape, reproduction in animals, and neuropeptides play an important role in locomotion. In this study, the function of pedal peptide-type neuropeptide (PDP) in the process of locomotor behavior of the sea cucumber Apostichopus japonicus was evaluated. The locomotor behavior of A. japonicus was recorded by infrared camera before and after PDP administration, and muscle physiology was studied by ultra performance liquid chromatography and quadrupole time-off-light mass spectrometry (UPLC-Q-TOF-MS) to clarify the potential physiological mechanisms. The results showed that PDP enhanced the cumulative duration of moving significantly at the 7th h after injection, and reduced the mean and maximum velocity by 16.90 and 14.22% in A. japonicus. The data of muscle metabolomics suggested that some significantly changed metabolites were related to locomotor behavior of sea cucumbers. The decreases of phosphatidylethanolamine (PE) and phosphatidylcholine (PC) might result in the increases of lysophosphatidylcholines (lysoPC) and lysophosphatidylethanolamine (lysoPE), and suggested the change of fluidity and permeability in the muscle cell membrane, which would affect the physiology and function of muscle cells, and finally alter the locomotor behavior. In addition, the increased level of arachidonic acid (ARA) might activate K+ ion channels and then affect the signaling of muscle cells, or promote the sensitivity of muscle cells to Ca2+ and then result in the contractility of longitudinal muscles in sea cucumbers. ARA was also involved in the linoleic acid metabolism which was the only pathway that disturbed significantly after PDP administration. In conclusion, PDP participated in the regulation of locomotor behavior in the sea cucumber, and the decreased PE and PC, increased lysoPC, lysoPE and ARA might be the potential physiological mechanisms that responsible for behavioral effects of PDP in A. japonicus.

Project description:BACKGROUND: Sea cucumbers are a special group of marine invertebrates. They occupy a taxonomic position that is believed to be important for understanding the origin and evolution of deuterostomes. Some of them such as Apostichopus japonicus represent commercially important aquaculture species in Asian countries. Many efforts have been devoted to increasing the number of expressed sequence tags (ESTs) for A. japonicus, but a comprehensive characterization of its transcriptome remains lacking. Here, we performed the large-scale transcriptome profiling and characterization by pyrosequencing diverse cDNA libraries from A. japonicus. RESULTS: In total, 1,061,078 reads were obtained by 454 sequencing of eight cDNA libraries representing different developmental stages and adult tissues in A. japonicus. These reads were assembled into 29,666 isotigs, which were further clustered into 21,071 isogroups. Nearly 40% of the isogroups showed significant matches to known proteins based on sequence similarity. Gene ontology (GO) and KEGG pathway analyses recovered diverse biological functions and processes. Candidate genes that were potentially involved in aestivation were identified. Transcriptome comparison with the sea urchin Strongylocentrotus purpuratus revealed similar patterns of GO term representation. In addition, 4,882 putative orthologous genes were identified, of which 202 were not present in the non-echinoderm organisms. More than 700 simple sequence repeats (SSRs) and 54,000 single nucleotide polymorphisms (SNPs) were detected in the A. japonicus transcriptome. CONCLUSION: Pyrosequencing was proven to be efficient in rapidly identifying a large set of genes for the sea cucumber A. japonicus. Through the large-scale transcriptome sequencing as well as public EST data integration, we performed a comprehensive characterization of the A. japonicus transcriptome and identified candidate aestivation-related genes. A large number of potential genetic markers were also identified from the A. japonicus transcriptome. This transcriptome resource would lay an important foundation for future genetic or genomic studies on this species.

Project description:Host-intestine microbiota interactions have been widely studied in aquatic animals, but these interactions in the intestine regeneration process of the sea cucumber Apostichopus japonicus have been rarely investigated. To understand how intestine regeneration impacts the developing intestinal microbiome composition and function, we performed a case study to characterize the intestinal microbial composition and functional genes of A. japonicus during intestine regeneration stages. High-throughput 16S rRNA gene sequencing revealed significantly different intestine microbiota compositions in different regeneration stages. The phylogenetic diversity and composition of the intestinal microbiota changed significantly in the early regeneration stage and tended to recover in the end stage. During the regeneration process, the abundance of Bacteroidetes and Rhodobacterales increased significantly. A network analysis revealed that Rhodobacteraceae and Flavobacteriaceae may function as keystone taxa in the intestinal microbial community of A. japonicus during intestine regeneration. Metagenomic analyses of representative samples revealed that the microbiomes of regenerating intestines were enriched in genes facilitating cell proliferation, digestion and immunity. The increased abundance of Bacteroidetes elevated the enrichment of genes associated with carbohydrate utilization. Some functional features in the subsystem category changed in a pattern that was consistent with the changing pattern of microbiota composition during intestine regeneration. Our results revealed that seemingly regular alterations in the intestinal microbiome composition and function are associated with intestine regeneration stages. Intestinal microbiota can increase the abundance of beneficial bacterial members and upregulate related functional genes to adapt to intestine regeneration and reconstruct a stable community structure. This study provides a new insight into the mechanism of the host-microbiota interaction response to organ regeneration.

Project description:Organisms respond to severe environmental changes by entering into hypometabolic states, minimizing their metabolic rates, suspending development and reproduction, and surviving critical ecological changes. They come back to an active lifestyle once the environmental conditions are conducive. Marine invertebrates live in the aquatic environment and adapt to environmental changes in their whole life. Sea cucumbers and sponges are only two recently known types of marine organisms that aestivate in response to temperature change. Sea cucumber has become an excellent model organism for studies of environmentally-induced aestivation by marine invertebrates. DNA methylation, the most widely considered epigenetic marks, has been reported to contribute to phenotypic plasticity in response to environmental stress in aquatic organisms. Most of methylation-related enzymes, including DNA methyltransferases, Methyl-CpG binding domain proteins, and DNA demethylases, were up-regulated during aestivation. We conducted high-resolution whole-genome bisulfite sequencing of the intestine from sea cucumber at non-aestivation and deep-aestivation stages. Further DNA methylation profile analysis was also conducted across the distinct genomic features and entire transcriptional units. A different elevation in methylation level at internal exons was observed with clear demarcation of intron/exon boundaries during transcriptional unit scanning. The lowest methylation level occurs in the first exons, followed by the last exons and the internal exons. A significant increase in non-CpG methylation (CHG and CHH) was observed within the intron and mRNA regions in aestivation groups. A total of 1393 genes were annotated within hypermethylated DMRs (differentially methylated regions), and 749 genes were annotated within hypomethylated DMRs. Differentially methylated genes were enriched in the mRNA surveillance pathway, metabolic pathway, and RNA transport. Then, 24 hypermethylated genes and 15 hypomethylated genes were Retrovirus-related Pol polyprotein from transposon (RPPT) genes. This study provides further understanding of epigenetic control on environmental induced hypometabolism in aquatic organisms.

Dataset Information

Neuropeptide precursors and neuropeptides in the sea cucumber Apostichopus japonicus: a genomic, transcriptomic and proteomic analysis.

Publications

Neuropeptide precursors and neuropeptides in the sea cucumber Apostichopus japonicus: a genomic, transcriptomic and proteomic analysis.

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