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Sci Rep
2020 Feb 03;101:1697. doi: 10.1038/s41598-020-58643-x.
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Integrated metabolomic and transcriptomic analyses identify critical genes in eicosapentaenoic acid biosynthesis and metabolism in the sea urchin Strongylocentrotus intermedius.
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Gonads are the only edible part of the sea urchin and have great potential as a health-promoting food for human consumption. Polyunsaturated fatty acids (PUFAs) are important necessary nutrients that determine not only the nutritional value of sea urchins but guarantee their normal growth and reproduction. However, the information on the molecular mechanisms of PUFA biosynthesis and metabolism in this species remains elusive. In this study, we used Strongylocentrotus intermedius as our model species and conducted integrated metabolomic and transcriptomic analyses of potentially critical genes involved in PUFA biosynthesis and metabolism during gonad growth and development, mainly focusing on eicosapentaenoic acid (EPA). We found six differentially accumulated metabolites associated with PUFA in the metabolomic analysis. More differentially expressed genes (DEGs) were related to PUFA in testis than ovary (1823 DEGs in testis and 1499 DEGs in ovary). We verified 12 DEGs by RNA-Seq results and found that Aldh7a1, Ecm3, Fads2, and Hsd17b12 genes had similar expression patterns in EPA concentration during gonad growth and development. In contrast, the other DEGs were downregulated and we inferred that EPA or PUFA may be metabolized as energy during certain periods. Our metabolic and genetic data will facilitate a better understanding of PUFA regulation networks during gonad growth and development in S. intermedius.
Figure 1. Changes of body size and weight in the sea urchin Strongylocentrotus intermedius, which was sampled for RNA and metabolite extraction. (A) Shell size; (B) wet weight and gonad somatic index (GSI) of sea urchin changes during gonad development stages. The results are expressed as meanâ±âSEM (nâ=â6).
Figure 2. Histological features of the sea urchin Strongylocentrotus intermedius gonads at different gonad development stages. Paraffin-embedded sections were stained with hematoxylin and eosin (HE). Stage 1: A, D; stage 2: B, E; stage 3: C, F. Scale bar: 200 μm.
Figure 3. Principal component analysis (PCA) score plots of sea urchin gonads in positive and negative ion modes. Ost1: ovary at stage 1; Ost2: ovary at stage 2; Ost3: ovary at stage 3; Tst1: testis at stage 1; Tst2: testis at stage 2; Tst3: testis at stage 3; QC: quality control (nâ=â6).
Figure 4. The differentially expressed genes (DEGs) related to eicosapentaenoic acid (EPA) during the gonad development of Strongylocentrotus intermedius. The DEGs are detected in three groups: Ost1 vs Ost3 (A), Ost2 vs Ost3 (B), and Tst1 vs Tst3 (C), respectively. Ost1: ovary at stage 1; Ost2: ovary at stage 2; Ost3: ovary at stage 3; Tst1: testis at stage 1; Tst3: testis at stage 3. The DEGs in the red circles represent upregulated genes and the DEGs in the blue circle represent downregulated genes.
Figure 5. Functional classification of the differentially expressed genes (DEGs) in Strongylocentrotus intermedius by using Kyoto Encyclopedia of Genes and Genomes (KEGG) terms. The DEGs are detected in three groups: Ost1 vs Ost3 (A), Ost2 vs Ost3 (B), and Tst1 vs Tst3 (C), respectively. Ost1: ovary at stage 1; Ost2: ovary at stage 2; Ost3: ovary at stage 3; Tst1: testis at stage 1; Tst3: testis at stage 3.
Figure 6. Quantitative (q)RT-PCR validation of the genes related to eicosapentaenoic acid (EPA) were differentially expressed among the different sexes and different development stages of the gonads. The relative expression of each gene were normalized to 18âS rRNA gene. Bars represent the meanâ±âSEM (nâ=â3). Ost1: ovary at stage 1; Ost2: ovary at stage 2; Ost3: ovary at stage 3; Tst1: testis at stage 1; Tst2: testis at stage 2;Tst3: testis at stage 3.
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