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Functional characterization of a Δ5-like fatty acyl desaturase and its expression during early embryogenesis in the noble scallop Chlamys nobilis Reeve

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Abstract

Long-chain polyunsaturated fatty acids (LC-PUFAs) are essential in lots of important physiological processes, while, many marine species have no or limited ability of endogenous PUFA biosynthesis, normally due to the lack of key enzymes such as fatty acid desaturase (FAD). In this study, we isolated a scallop Chlamys nobilis cDNA with high homology to vertebrate FADs. Functional characterization in recombinant yeast Saccharomyces cerevisiae showed that scallop FAD exhibited Δ5-desaturation activity towards both saturated and PUFA substrates. Thus, it efficiently desaturated exogenously added PUFA C20:4(n − 3) and C20:3(n − 6) to C20:5(n − 3) (EPA) and C20:4(n − 6) (ARA) respectively. It also converted the yeast’s endogenous C18:0 into C18:1(n − 13), and participated in the biosynthesis of non-methylene-interrupted FA by introducing a double bond to C20:3(n − 3) and C20:2(n − 6) in the Δ5 carbon. Temporal transcript profile of scallop FAD was studied during early embryonic development. High level of mRNA was found at the beginning of embryogenesis (egg) and noticeable decreases of were observed during larvae development, suggesting maternal FAD mRNA transfer to the embryo. Further, FAD transcripts were detected in all tissues analyzed, with the gonad and hepatopancreas showing the highest expression.

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References

  1. Neuringer M, Anderson GJ, Connor WE (1988) The essentiality of n − 3 fatty acids for the development and function of the retina and brain. Annu Rev Nutr 8(1):517–541

    Article  PubMed  CAS  Google Scholar 

  2. Lands WE (1993) Eicosanoids and health. Ann NY Acad Sci 676(1):46–59

    Article  PubMed  CAS  Google Scholar 

  3. Graham I, Cirpus P, Rein D, Napier J (2004) The use of very long chain polyunsaturated fatty acids to ameliorate metabolic syndrome: transgenic plants as an alternative sustainable source to fish oils. Nutr Bull 29(3):228–233

    Article  Google Scholar 

  4. Nugent AP (2004) The metabolic syndrome. Nutr Bull 29(1):36–43

    Article  Google Scholar 

  5. Hastings N, Agaba M, Tocher DR, Leaver MJ, Dick JR, Sargent JR, Teale AJ (2001) A vertebrate fatty acid desaturase with Δ5 and Δ6 activities. Proc Natl Acad Sci USA 98(25):14304–14309

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  6. Li Y, Monroig O, Zhang L, Wang S, Zheng X, Dick JR, You C, Tocher DR (2010) Vertebrate fatty acyl desaturase with Δ4 activity. Proc Natl Acad Sci USA 107(39):16840–16845

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Castro LFC, Monroig O, Leaver MJ, Wilson J, Cunha I, Tocher DR (2012) Functional desaturase Fads1 (Δ5) and Fads2 (Δ6) orthologues evolved before the origin of jawed vertebrates. PLoS One 7(2):e31950

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  8. Monroig Ó, Tocher DR, Hontoria F, Navarro JC (2013) Functional characterisation of a Fads2 fatty acyl desaturase with Δ6/Δ8 activity and an Elovl5 with C16, C18 and C20 elongase activity in the anadromous teleost meagre (Argyrosomus regius). Aquaculture 412:14–22

    Article  Google Scholar 

  9. Monroig Ó, Navarro JC, Dick JR, Alemany F, Tocher DR (2012) Identification of a Δ5-like fatty acyl desaturase from the cephalopod Octopus vulgaris (Cuvier 1797) involved in the biosynthesis of essential fatty acids. Mar Biotechnol 14(4):411–422

    Article  PubMed  CAS  Google Scholar 

  10. Li M, Mai K, He G, Ai Q, Zhang W, Xu W, Wang J, Liufu Z, Zhang Y, Zhou H (2013) Characterization of two Δ5 fatty acyl desaturases in abalone (Haliotis discus hannai Ino). Aquaculture 416:48–56

    Article  Google Scholar 

  11. Waldock M, Holland D (1984) Fatty acid metabolism in young oysters, Crassostrea gigas: polyunsaturated fatty acids. Lipids 19(5):332–336

    Article  CAS  Google Scholar 

  12. Chu FL, Greaves J (1991) Metabolism of palmitic, linoleic, and linolenic acids in adult oysters, Crassostrea virginica. Mar Biol 110(2):229–236

    Article  CAS  Google Scholar 

  13. Zhukova NV (1991) The pathway of the biosynthesis of non-methylene-interrupted dienoic fatty acids in molluscs. Comp Biochem Physiol B 100(4):801–804

    Article  Google Scholar 

  14. Zhukova N, Svetashev V (1986) Non-methylene-interrupted dienoic fatty acids in molluscs from the sea of Japan. Comp Biochem Physiol B 83(3):643–646

    Google Scholar 

  15. Caers M, Coutteau P, Sorgeloos P, Gajardo G (2003) Impact of algal diets and emulsions on the fatty acid composition and content of selected tissues of adult broodstock of the Chilean scallop Argopecten pupuratus (Lamarck, 1819). Aquaculture 217(1):437–452

    Article  CAS  Google Scholar 

  16. Da Costa F, Nóvoa S, Ojea J, Martínez-Patiño D (2012) Effects of algal diets and starvation on growth, survival and fatty acid composition of Solen marginatus (Bivalvia: Solenidae) larvae. Sci Mar 76(3):527–537

    Article  Google Scholar 

  17. Zheng H, Liu H, Zhang T, Wang S, Sun Z, Liu W, Li Y (2010) Total carotenoid differences in scallop tissues of Chlamys nobilis (Bivalve: Pectinidae) with regard to gender and shell colour. Food Chem 122(4):1164–1167

    Article  CAS  Google Scholar 

  18. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

    Article  PubMed  CAS  Google Scholar 

  19. Morais S, Monroig O, Zheng X, Leaver MJ, Tocher DR (2009) Highly unsaturated fatty acid synthesis in Atlantic salmon: characterization of ELOVL5- and ELOVL2-like elongases. Mar Biotechnol 11(5):627–639

    Article  PubMed  CAS  Google Scholar 

  20. Agaba M, Tocher DR, Dickson CA, Dick JR, Teale AJ (2004) Zebrafish cDNA encoding multifunctional fatty acid elongase involved in production of eicosapentaenoic (20:5n − 3) and docosahexaenoic (22:6n − 3) acids. Mar Biotechnol 6(3):251–261

    Article  PubMed  CAS  Google Scholar 

  21. Sperling P, Ternes P, Zank TK, Heinz E (2003) The evolution of desaturases. Prostaglandins Leukot Essent 68(2):73–95

    Article  CAS  Google Scholar 

  22. Watts JL (2002) Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc Natl Acad Sci USA 99(9):5854–5859

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  24. Ge L, Gordon JS, Hsuan C, Stenn K, Prouty SM (2003) Identification of the Δ6 desaturase of human sebaceous glands: expression and enzyme activity. J Invest Dermatol 120(5):707–714

    Article  PubMed  CAS  Google Scholar 

  25. Berthelin C, Kellner K, Mathieu M (2000) Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (West Coast of France). Comp Biochem Physiol B 125(3):359–369

    Article  PubMed  CAS  Google Scholar 

  26. Monroig Ó, Rotllant J, Sánchez E, Cerdá-Reverter JM, Tocher DR (2009) Expression of long-chain polyunsaturated fatty acid (LC-PUFA) biosynthesis genes during zebrafish Danio rerio early embryogenesis. BBA-Mol Cell Biol Lipids 1791(11):1093–1101

    Article  CAS  Google Scholar 

  27. Bell JG, Sargent JR (2003) Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture 218(1):491–499

    Article  CAS  Google Scholar 

  28. Helm M, Holland D, Stephenson R (1973) The effect of supplementary algal feeding of a hatchery breeding stock of Ostrea edulis L. on larval vigour. J Mar Biol Assoc UK 53:673–684

    Article  Google Scholar 

  29. Jonsson P, Berntsson K, André C, Wängberg S-Å (1999) Larval growth and settlement of the European oyster (Ostrea edulis) as a function of food quality measured as fatty acid composition. Mar Biol 134(3):559–570

    Article  CAS  Google Scholar 

  30. Miliou H, Fintikaki M, Tzitzinakis M, Kountouris T, Verriopoulos G (2006) Fatty acid composition of the common octopus, Octopus vulgaris, in relation to rearing temperature and body weight. Aquaculture 256(1):311–322

    Article  CAS  Google Scholar 

  31. Helm M, Laing I (1987) Preliminary observations on the nutritional value of Tahiti Isochrysis to bivalve larvae. Aquaculture 62(3):281–288

    Article  Google Scholar 

  32. Gallager SM, Mann R (1986) Growth and survival of larvae of Mercenaria mercenaria (L.) and Crassostrea virginica (Gmelin) relative to broodstock conditioning and lipid content of eggs. Aquaculture 56(2):105–121

    Article  CAS  Google Scholar 

  33. Koven W, Barr Y, Lutzky S, Ben-Atia I, Weiss R, Harel M, Behrens P, Tandler A (2001) The effect of dietary arachidonic acid (20:4n-6) on growth, survival and resistance to handling stress in gilthead seabream (Sparus aurata) larvae. Aquaculture 193(1):107–122

    CAS  Google Scholar 

  34. Hendriks IE, van Duren LA, Herman PM (2003) Effect of dietary polyunsaturated fatty acids on reproductive output and larval growth of bivalves. J Exp Mar Biol Ecol 296(2):199–213

    Article  CAS  Google Scholar 

  35. Liu H, Zheng H, Wang S, Wang Y, Li S, Liu W, Zhang G (2013) Cloning and functional characterization of a polyunsaturated fatty acid elongase in a marine bivalve noble scallop Chlamys nobilis Reeve. Aquaculture 416:146–151

    Article  Google Scholar 

  36. Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Yang P, Zhang L, Wang X, Qi H (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490(7418):49–54

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. Chiju Wei (Multidisciplinary Research Center, Shantou University) for reviewing our manuscript. Funding for this research was provided by China Modern Agro-industry Technology Research System (CARS-48), Ministry of Education of P. R. China (20114402110001), National Natural Science Foundation of China (41076107, 31372528), Department of Education (GCZX–A0908, 2050205–95) and Department of Science & Technology (2011B090400040, 2012NL048) of Guangdong Province, China.

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Authors and Affiliations

  1. Key Laboratory of Marine Biotechnology of Guangdong Province, Shantou University, Shantou, 515063, China

    Helu Liu, Zhicheng Guo, Huaiping Zheng, Shuqi Wang, Yajun Wang & Wenhua Liu

  2. Department of Education of Guangdong Province, Mariculture Research Center for Subtropical Shellfish & Algae, Shantou, 515063, China

    Helu Liu, Zhicheng Guo, Huaiping Zheng, Shuqi Wang, Yajun Wang & Wenhua Liu

  3. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Guofan Zhang

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  1. Helu Liu
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  2. Zhicheng Guo
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  3. Huaiping Zheng
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Correspondence to Huaiping Zheng.

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Liu, H., Guo, Z., Zheng, H. et al. Functional characterization of a Δ5-like fatty acyl desaturase and its expression during early embryogenesis in the noble scallop Chlamys nobilis Reeve. Mol Biol Rep 41, 7437–7445 (2014). https://doi.org/10.1007/s11033-014-3633-4

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  • DOI: https://doi.org/10.1007/s11033-014-3633-4

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