Integrated metabolomic and transcriptomic analyses identify critical genes in eicosapentaenoic acid biosynthesis and metabolism in the sea urchin Strongylocentrotus intermedius

Abstract

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. The gonads which produce roe are the only edible part of the sea urchins and have great potential to promote benfites to human health 1,2. The sea urchin gonads have high nutritional value and possess several essential nutrients like protein, lipids, polysaccharides, fatty acids, minierlas and vitamins. Polyunsaturated fatty acids (PUFAs) are one of ' the most important and necessary nutrients, with eicosapentaenoic acid (EPA) as the main component among the PUFAs. Many biophysical studies have revealed that PUFAs significantly alter the basic properties of membranes such as acyl chain order, fluidity, elastic compressibility, phase behavior and permeability 3,4 , and play a beneficial role in stabilizing dynamic membrane 5 , membrane organization and cell division 6. In addition, some PUFAs have significant influence on the production of eicosanoids, which involved in the body's inflammatory response and homeostatic processes, neurological disorders, and cardiovascular diseases 7,8. The potential of PUFA in stimulating bone, brain and immune cell development at embryonic through to early phases of the animal's life could significantly improve productivity and welfare 9. In marine invertebrates, PUFAs play a key role in metabolic health and influence various cellular processes, such as serving as a repository for energy reserves or regulating gene expression of metabolic disorders 10. It is believed that PUFAs could be synthesized in marine invertebrates 11 , such as mollusks, in which the biosynthesis of PUFA has been most extensively investigated 12. However, unlike vertebrates, information on

De novo Assembly and Analysis of Tissue-Specific Transcriptomes of the Edible Red Sea Urchin Loxechinus albus Using RNA-Seq

“…In addition, a gonadal transcriptomic of M. nudus present candidate sex-related genes that could be involved in significant roles in spermatogenesis, oogenesis, and germ cell development [52]. More recently, integrated analyses of metabolomic and transcriptomic reveal key genes for metabolism and eicosapentaenoic acid biosynthesis in the sea urchin S. intermedius, identifying six accumulated metabolites and several differentially expressed genes associated with polyunsaturated fatty acids in the testis compared with the ovary [53].…”

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“…Such integration techniques provide a deeper understanding of the molecular mechanisms involved in the production of biologically active compounds through the identification of BGCs, gene expression patterns and enzymes related to the produced metabolites (Paul et al, 2019;van der Hooft et al, 2020). For example, an integrated metabolomic-transcriptomic analysis of the sea urchin Strongylocentrotus intermedius allowed identification of critical genes related to eicosanoid acid biosynthesis (Wang et al, 2020). A study of Dysideidae sponges using mass spectrometry, molecular fragmentation and NMR spectroscopy identified a large-array of new polybrominated diphenyl ethers (PBDEs) in these sponges (Agarwal et al, 2015).…”