Skip to main content
Log in

De novo transcriptomic analysis of gonad of Strongylocentrotus nudus and gene discovery for biosynthesis of polyunsaturated fatty acids

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Background

Strongylocentrotus nudus is an important cultured sea urchin species in north China, because its gonad is rich in unsaturated fatty acids, particularly long polyunsaturated fatty acids (LC-PUFAs). These PUFAs play pleiotropic and crucial roles in a wide range of biological process.

Objective

However, the genes contributing to biosynthesis PUFAs have not been elucidated yet, and the molecular mechanism relative to the difference in PUFA composition between male and female gonad as been revealed but the corresponding has not been understood.

Methods

In this paper, solexa sequencing based transcriptomic approach was used to identify and characterize the key genes relative to PUFA synthesis and further conducted different expressed genes between male and female gonad.

Results

A total of 130,124 transcripts and 189330 unigenes were de novo assembled from 64.32 Gb data. Next, these unigenes were subjected to functional annotation by mapping to six public databases, and this process revealed a lot of genes involving in lipid metabolism. In addition, three types of fatty acids front-end desaturase and three species of very long fatty acids elongase were identified and the pathway for PUFA biosynthesis was hypothesized. Last, comparative analysis revealed the higher expression level of Δ5 desaturase, Δ6 desaturase, ELOVL-4, -6 and -7 in male gonad compared with female.

Conclusion

This results could plausible explain the differ in composition of PUFAs between male and female gonad of sea urchin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Barnathan G (2009) Non-methylene-interrupted fatty acids from marine invertebrates: Occurrence, characterization and biological properties. Biochimie 91(6):671–678

    Article  CAS  PubMed  Google Scholar 

  • Bazinet RP, Layé S (2014) Polyunsaturated fatty acids and their metabolites in brain function and disease. Nat Rev Neurosci 15:771–785

    Article  CAS  PubMed  Google Scholar 

  • Beeble A, Calestani C (2012) Expression pattern of polyketide synthase-2 during sea urchin development. Gene Expr Patterns 12(1–2):7–10

    Article  CAS  PubMed  Google Scholar 

  • Bell MV, Dick JR, Kelly MS (2001) Biosynthesis of eicosapentaenoic acid in the sea urchin Psammechinus miliaris. Lipids 36(1):79–82

    Article  CAS  PubMed  Google Scholar 

  • Billerey C, Boussaha M, Esquerré D et al (2014) Identification of large intergenic non-coding RNAs in bovine muscle using next-generation transcriptomic sequencing. BMC Genom. https://doi.org/10.1186/1471-2164-15-499

    Article  Google Scholar 

  • Bookbinder LH, Shick JM (1986) Anaerobic and aerobic energy metabolism in ovaries of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 93(1):103–110

    Article  CAS  Google Scholar 

  • Bulgakov AA, Eliseikina MG, Kovalchuk SN et al (2013) Mannan-binding lectin of the sea urchin Strongylocentrotus nudus. Mar Biotechnol (NY) 15(1):73–86

    Article  CAS  Google Scholar 

  • Carboni S, Hughes AD, Atack T et al (2013) Fatty acid profiles during gametogenesis in sea urchin (Paracentrotus lividus): effects of dietary inputs on gonad, egg and embryo profiles. Comp Biochem Physiol A Mol Integr Physiol 164(2):376–382

    Article  CAS  PubMed  Google Scholar 

  • Castoe TA, Stephens T, Noonan BP, Calestani C (2007) A novel group of type I polyketide synthases (PKS) in animals and the complex phylogenomics of PKSs. Gene 392(1–2):47–58

    Article  CAS  PubMed  Google Scholar 

  • Castro LFC, Monroig O, Leaver MJ et al (2012) Functional desaturase Fads1 (∆5) and Fads2 (∆6) orthologues evolved before the origin of jawed vertebrates. PLoS One. https://doi.org/10.1371/journal.pone.0031950

    Article  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Corominas J, Ramayo-Caldas Y, Puig-Oliveras A et al (2013) Analysis of porcine adipose tissue transcriptome reveals differences in de novo fatty acid synthesis in pigs with divergent muscle fatty acid composition. BMC Genom. https://doi.org/10.1186/1471-2164-14-843

    Article  Google Scholar 

  • Della Sala G, Hochmuth T, Costantino V et al (2013) Polyketide genes in the marine sponge Plakortis simplex: a new group of mono-modular type I polyketide synthases from sponge symbionts. Environ Microbiol Rep 5(6):809–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding J, Chang YQ, Hao ZL, Zhang B (2011) Comparative studies on urchin in gonad fatty acid composition and β-carotene content in north china sea section. J Agric Sci Technol 13(3):122–128

    CAS  Google Scholar 

  • Djebali S, Davis CA, Merkel A et al (2012) Landscape of transcription in human cells. Nature 489(7414):101–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodge CA, Edwards MS (2012) Seasonal variation in the effects of food availability on gametogenesis in the purple urchin (Strongylocentrotus purpuratus). Mar Biol 159(2):427–433

    Article  Google Scholar 

  • Du H, Bao Z, Hou R et al (2012) Transcriptome sequencing and characterization for the sea cucumber Apostichopus japonicus (Selenka,1867). PLoS One. https://doi.org/10.1371/journal.pone.0033311

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng LF, Huang XX, Wen W et al (2012) Changes in lipid characteristics and fatty acid contents of developmental yolk-sac larvae of Epinephelus awoara and Trachinotus ovatus. J Shanghai Ocean Univ 21(5):720–727

    Google Scholar 

  • Fonseca-Madrigal J, Navarro JC, Hontoria F et al (2014) Diversification of substrate specificities in teleostei Fads2: characterization of ∆4 and ∆6∆5 desaturases of Chirostoma estor. J Lipid Res 55(7):1408–1419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francis WR, Christianson LM, Kiko R et al (2013) A comparison across non-model animals suggests an optimal sequencing depth for de novo transcriptome assembly. BMC Genom. https://doi.org/10.1186/1471-2164-14-167

    Article  Google Scholar 

  • Goel M, Mushegian A (2006) Intermediary metabolism in sea urchin: the first inferences from the genome sequence. Dev Biol 300(1):282–292

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29(7):644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M et al (2013) De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nat Protoc 8(8):1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto K, Yoshizawa AC, Okuda S et al (2008) The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes. J Lipid Res 49(1):183–191

    Article  CAS  PubMed  Google Scholar 

  • Holder T, Basquin C, Ebert J et al (2013) Deep transcriptome-sequencing and proteome analysis of the hydrothermal vent annelid Alvinella pompejana identifies the CvP-bias as a robust measure of eukaryotic thermostability. Biol Direct. https://doi.org/10.1186/1745-6150-8-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Hou R, Bao Z, Wang S et al (2011) Transcriptome sequencing and de novo analysis for Yesso scallop (Patinopecten yessoensis) using 454 GS FLX. PLoS One. https://doi.org/10.1371/journal.pone.0021560

    Article  PubMed  PubMed Central  Google Scholar 

  • Houk MS, Hinegardner RT (1980) The formation and early differentiation of sea urchin gonads. Biol Bull 159(2):280–294

    Article  Google Scholar 

  • Itabashi Y, Kunagai M, Ota T, Nakao H (1998) Fatty acid composition of the gonad of the sea urchin Strongylocentrotus nudus fed Fish. J Jpn Oil Chem Soc 47(7):703–707,718

    Article  CAS  Google Scholar 

  • Jakhesara SJ, Koringa PG, Joshi CG (2013) Identification of novel exons and transcripts by comprehensive RNA-Seq of horn cancer transcriptome in Bos indicus. J Biotechnol 165(1):37–44

    Article  CAS  PubMed  Google Scholar 

  • Jin S, Fu H, Zhou Q et al (2013) Transcriptome analysis of androgenic gland for discovery of novel genes from the oriental river prawn, Macrobrachium nipponense, using Illumina Hiseq 2000. PLoS One. https://doi.org/10.1371/journal.pone.0076840

    Article  PubMed  PubMed Central  Google Scholar 

  • Kelly JR, Scheibling RE, Iverson SJ, Gagnon P (2008) Fatty acid profiles in the gonads of the sea urchin Strongylocentrotus droebachiensis on natural algal diets. Mar Ecol Prog Ser 373:1–9

    Article  CAS  Google Scholar 

  • Kornprobst JM, Barnathan G (2010) Demospongic acids revisited. Mar Drugs 8(10):2569–2577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lands B (2014) Historical perspectives on the impact of n-3 and n-6 nutrients on health. Prog Lipid Res 55:17–29

    Article  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Li D, Deng Z, Qin B et al (2012) De novo assembly and characterization of bark transcriptome using Illumina sequencing and development of EST-SSR markers in rubber tree (Hevea brasiliensis Muell. Arg.). BMC Genom. https://doi.org/10.1186/1471-2164-13-192

    Article  Google Scholar 

  • Li M, Mai K, He G et al (2013) Characterization of two ∆5 fatty acyl desaturases in abalone (Haliotis discus hannai Ino). Aquaculture 416:48–56

    Article  CAS  Google Scholar 

  • Lin Q, Li S, Dong W et al (2015) Involvement of CitCHX and CitDIC in developmental- related and postharvest-hot-air driven citrate degradation in Citrus fruits. PLoS One. https://doi.org/10.1371/journal.pone.0119410

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu H, Guo Z, Zheng H et al (2014a) Functional characterization of a ∆5-like fatty acyl desaturase and its expression during early embryogenesis in the noble scallop Chlamys nobilis Reeve. Mol Biol Rep 41(11):7437–7445

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Zhang H, Zheng H et al (2014b) PUFA biosynthesis pathway in marine Scallop Chlamys nobilis Reeve. J Agric Food Chem 62(51):12384–12391

    Article  CAS  PubMed  Google Scholar 

  • Makarenko I, Selezneva AI, Pozharitskaya ON et al (2013) Effects of lipid extract of sea urchins gonads in metabolic syndrome animal model. Planta Med. https://doi.org/10.1055/s-0033-1351989

    Article  Google Scholar 

  • Marioni JC, Mason CE, Mane SM et al (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18(9):1509–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez I, García FJ, Sánchez AI et al (2003) Biometric parameters and reproductive cycle of Paracentrotus lividus (Lamarck) in three habitats of Southern Spain. In: Feral JP, David B (eds) Echinoderm research 2001. Swets and Zeitlinger, Lisse

    Google Scholar 

  • Martínez-Pita I, García FJ, Pita ML (2010) Males and females gonad fatty acids of the sea urchins Paracentrotus lividus and Arbacia lixula (Echinodermata). Helgol Mar Res 64:135–142

    Article  Google Scholar 

  • Meesapyodsuk D, Qiu X (2012) The Front-end desaturase: structure, function, evolution and biotechnological use. Lipids 47(3):227–237

    Article  CAS  PubMed  Google Scholar 

  • Meyer E, Aglyamova GV, Wang S et al (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genom. https://doi.org/10.1186/1471-2164-10-219

    Article  Google Scholar 

  • Monroig O, Zheng X, Morais S et al (2010) Multiple genes for functional 6 fatty acyl desaturases (Fad) in Atlantic salmon (Salmo salar L.): gene and cDNA characterization, functional expression, tissue distribution and nutritional regulation. Biochim Biophys Acta 1801(9):1072–1081

    Article  CAS  PubMed  Google Scholar 

  • Monroig O, Navarro JC, Tocher DR (2011) Long-chain polyunsaturated fatty acids in fish: recent advances on desaturases and elongases involved in their biosynthesis. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Nieto-López MG, Villarreal-Cavazos DA, Gamboa-Delgado J, Hernández-Hernández L (eds) Avances en Nutrición Acuícola XI-Memorias del Décimo Primer Simposio Internacional de Nutrición Acuícola. Universidad Autónoma de Nuevo León, México

    Google Scholar 

  • Monroig O, Navarro JC, Dick JR et al (2012) Identification of a ∆5-like fatty acyl desaturase from the cephalopod Octopus vulgaris (Cuvier 1797) involved in the biosynthesis of essential fatty acids. Mar Biotechnol (NY) 14(4):411–422

    Article  CAS  Google Scholar 

  • Monroig Ó, Tocher DR, Navarro JC (2013) Biosynthesis of polyunsaturated fatty acids in marine invertebrates: recent advances in molecular mechanisms. Mar Drugs 11(10):3998–4018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naganuma T, Sato Y, Sassa T et al (2011) Biochemical characterization of the very long-chain fatty acid elongase ELOVL7. FEBS Lett 585:3337–3341

    Article  CAS  PubMed  Google Scholar 

  • Oshlack A, Wakefield MJ (2009) Transcript length bias in RNA-seq data confounds systems biology. Biol Direct. https://doi.org/10.1186/1745-6150-4-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Pennisi E (2006) Sea urchin genome confirms kinship to humans and other vertebrates. Science 314(5801):908–909

    Article  CAS  PubMed  Google Scholar 

  • Puig-Oliveras A, Ramayo-Caldas Y, Corominas J et al (2014) Differences in muscle transcriptome among pigs phenotypically extreme for fatty acid composition. PLoS One 9(6):e99720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purdy JG, Shenk T, Rabinowitz JD (2015) Fatty acid elongase 7 catalyzes lipidome remodeling essential for human cytomegalovirus replication. Cell Rep 10(8):1375–1385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond JF, Himmelman JH, Guderley HE (2007) Biochemical content, energy composition and reproductive effort in the broadcasting sea star Asterias vulgaris over the spawning period. J Exp Mar Biol Ecol 341:32–44

    Article  Google Scholar 

  • Raymond WW, Lowe AT, Galloway AWE (2014) Degradation state of algal diets affects fatty acid composition but not size of red urchin gonads. Mar Ecol Prog Ser 509:213–225

    Article  CAS  Google Scholar 

  • Rogowski MP, Flowers MT, Stamatikos AD et al (2013) SCD1 activity in muscle increases triglyceride PUFA content, exercise capacity, and PPARδ expression in mice. J Lipid Res 54(10):2636–2646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siriwardhana N, Kalupahana NS, Moustaid-Moussa N (2012) Health benefits of n-3 polyunsaturated fatty acids: eicosapentaenoic acid and docosahexaenoic acid. Adv Food Nutr Res 65:211–222

    Article  PubMed  Google Scholar 

  • Sun L, Zhang Z, Bailey TL et al (2012) Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. BMC Bioinform. https://doi.org/10.1186/1471-2105-13-331

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D et al (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong SY, Chen W, You XC et al (1998) Study on lipid and fatty acids composition of three kinds of Echinoidea’s gonad. J Fish China 22(3):247–252

    Google Scholar 

  • Tosi F, Sartori F, Guarini P et al (2014) Delta-5 and delta-6 desaturases: crucial enzymes in polyunsaturated fatty acid-related pathways with pleiotropic influences in health and disease. Adv Exp Med Biol 824:61–81

    Article  CAS  PubMed  Google Scholar 

  • Unuma T, Yamamoto T, Akiyama T et al (2003) Quantitative changes in yolk protein and other components in the ovary and testis of the sea urchin Pseudocentrotus depressus. J Exp Biol 206(Pt2):365–372

    Article  CAS  PubMed  Google Scholar 

  • Uttaro AD (2006) Biosynthesis of polyunsaturated fatty acids in lower eukaryotes. IUBMB Life 58(10):563–571

    Article  CAS  PubMed  Google Scholar 

  • Wathes DC, Abayasekara DR, Aitken RJ (2007) Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 77:190–201

    Article  CAS  PubMed  Google Scholar 

  • White NM, Cabanski CR, Silva-Fisher JM et al (2014) Transcriptome sequencing reveals altered long intergenic non-coding RNAs in lung cancer. Genome Biol. https://doi.org/10.1186/s13059-014-0429-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu K, Jia Z, Wang Q et al (2017) Identification, expression analysis, and the regulating function on C/EBPs of KLF10 in Dalian purple sea urchin, Strongylocentrotus nudus. Genome 60(10):837–849

    Article  CAS  PubMed  Google Scholar 

  • Xiang LX, He D, Dong WR et al (2010) Deep sequencing-based transcriptome profiling analysis of bacteria-challenged Lateolabrax japonicus reveals insight into the immune-relevant genes in marine fish. BMC Genom. https://doi.org/10.1186/1471-2164-11-472

    Article  Google Scholar 

  • Ye J, Fang L, Zheng H et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(Web Server issue):W293-297

    Google Scholar 

  • Zhu BW, Qin L, Zhou DY et al (2010) Extraction of lipid from sea urchin (Strongylocentrotus nudus) gonad by enzyme-assisted aqueous and supercritical carbon dioxide methods. Eur Food Res Technol 230(5):737–743

    Article  CAS  Google Scholar 

  • Zhukova NV (2014) Lipids and fatty acids of Nudibranch Mollusks: Potential sources of bioactive compounds. Mar Drugs 12(8):4578–4592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (Grant No. 31272704).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhenlin Wei.

Ethics declarations

Conflict of interest

The author declare that we have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, Z., Liu, X., Zhou, Z. et al. De novo transcriptomic analysis of gonad of Strongylocentrotus nudus and gene discovery for biosynthesis of polyunsaturated fatty acids. Genes Genom 41, 583–597 (2019). https://doi.org/10.1007/s13258-019-00799-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-019-00799-6

Keywords

Navigation