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RNA-Seq dependent transcriptional analysis unveils adaptive mechanisms in the intestine of sea cucumber Apostichopus japonicus during aestivation

ABSTRACT: Sea cucumbers (Holothuroidea; Echinodermata), cycle annually between aestivation when water temperature is above about 25°C in the summer and active life when temperature is below about 18°C. We used RNA-Seq to determine gene expression profiles of intestine tissue of A.japonicus during non-aestivation (NA), deep-aestivation (DA), and arousal from aestivation (AA).

ORGANISM(S): Apostichopus japonicus

PROVIDER: GSE51137 | GEO | 2015/08/08

SECONDARY ACCESSION(S): PRJNA221256

REPOSITORIES: GEO

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Project description:The sea cucumber Apostichopus japonicus withstands high water temperatures in the summer by suppressing metabolic rate and entering a state of aestivation. We hypothesized that changes in the expression of miRNAs could provide important post-transcriptional regulation of gene expression during hypometabolism via control over mRNA translation. The present study analyzed profiles of miRNA expression in the sea cucumber respiratory tree using Solexa deep sequencing technology. We identified 279 sea cucumber miRNAs, including 15 novel miRNAs specific to sea cucumber. Animals sampled during deep aestivation (DA; after at least 15 days of continuous torpor) were compared with animals from a non-aestivation (NA) state (animals that had passed through aestivation and returned to an active state). We identified 30 differentially expressed miRNAs ([RPM (reads per million) >10, |FC| (|fold change|) M-bM-^IM-%1, FDR (false discovery rate) <0.01]) during aestivation, which were validated by two other miRNA profiling methods: miRNA microarray and real-time PCR. Among the most prominent miRNA species, miR-124, miR-124-3p, miR-79, miR-9 and miR-2010 were significantly over-expressed during deep aestivation compared with non-aestivation animals, suggesting that these miRNAs may play important roles in metabolic rate suppression during aestivation. In the present study, an analysis of the global profile of small RNAs was conducted using Solexa sequencing technology in non-aestivation (NA) and deep aestivation (DA) sea cucumbers. We focus on respiratory tree in the present study because it is the important site responsible for the strong metabolic rate depression seen under deep aestivating conditions and the global expression profile of mRNA from the this organ has also been constructed applying RNA-seq technology in our previous study (Zhao and Chen, unpublished data). A preliminary analysis of the functional relevance of miRNA expression in relation to hypometabolism during aestivation is presented. A miRNA microarray and RT-qPCR were both used to supplement and confirm differentially expressed miRNAs. Our findings provide important new insights into the molecular mechanisms of sea cucumber aestivation.

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.

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RNA-Seq dependent transcriptional analysis unveils adaptive mechanisms in the intestine of sea cucumber Apostichopus japonicus during aestivation

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