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Fatty Acid and Lipid Profiles with Emphasis on n-3 Fatty Acids and Phospholipids from Ciona intestinalis

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Lipids

Abstract

In order to establish Ciona intestinalis as a new bioresource for n-3 fatty acids-rich marine lipids, the animal was fractionated into tunic and inner body tissues prior to lipid extraction. The lipids obtained were further classified into neutral lipids (NL), glycolipids (GL) and phospholipids (PL) followed by qualitative and quantitative analysis using GC-FID, GC–MS, 1H NMR, 2D NMR, MALDI-TOF-MS and LC–ESI–MS methods. It was found that the tunic and inner body tissues contained 3.42–4.08 % and 15.9–23.4 % of lipids respectively. PL was the dominant lipid class (42–60 %) irrespective of the anatomic fractions. From all lipid fractions and classes, the major fatty acids were 16:0, 18:1n-9, C20:1n-9, C20:5n-3 (EPA) and C22:6n-3 (DHA). The highest amounts of long chain n-3 fatty acids, mainly EPA and DHA, were located in PL from both body fractions. Cholestanol and cholesterol were the dominant sterols together with noticeable amounts of stellasterol, 22 (Z)-dehydrocholesterol and lathosterol. Several other identified and two yet unidentified sterols were observed for the first time from C. intestinalis. Different molecular species of phosphatidylcholine (34 species), sphingomyelin (2 species), phosphatidylethanolamine (2 species), phosphatidylserine (10 species), phosphatidylglycerol (9 species), ceramide (38 species) and lysophospholipid (5 species) were identified, representing the most systematic PL profiling knowledge so far for the animal. It could be concluded that C. intestinalis lipids should be a good alternative for fish oil with high contents of n-3 fatty acids. The lipids would be more bioavailable due to the presence of the fatty acids being mainly in the form of PL.

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Abbreviations

DHA:

Docosahexaenoic acid

EPA:

Eicosapentaenoic acid

MUFA:

Monounsaturated fatty acid(s)

PUFA:

Polyunsaturated fatty acid(s)

SFA:

Saturated fatty acid(s)

PtdCho:

Phosphatidylcholine

PtdSer:

Phosphatidylserine

PtdEtn:

Phosphoethanolamine

CerPCho:

Sphingomyelin

PtdGro:

Phosphatidylglycerols

Cer:

Ceramide

Lyso-PtdEtn:

Lysophosphatidylethanolamine

Lyso-PtdSer:

Lysophosphatidylserine

GC-FID:

Gas chromatography-flame ionization detector

GC–MS:

Gas chromatography mass spectrometry

MALDI-TOF-MS:

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

LC–ESI–MS:

Liquid chromatography electrospray ionization mass spectrometry

1H NMR:

One dimensional proton nuclear magnetic resonance

2D HSQC-NMR:

Two dimensional heteronuclear single quantum coherence nuclear magnetic resonance

References

  1. Millar RH (1953) Ciona. University Press, Liverpool

  2. Therriault TW, Herborg L-M (2008) A qualitative biological risk assessment for vase tunicate Ciona intestinalis in Canadian waters: using expert knowledge. ICES J Mar Sci 65:781–787

    Article  Google Scholar 

  3. Troedsson C, Thompson E, Schander C, Bouquet JM, Magnesen T, Li J (2011) Method of producing a biofuel from a tunicate or an extract obtained from a tunicate.WO2011158215A2

  4. Zhao Y, Li J (2014) Excellent chemical and material cellulose from tunicates: diversity in cellulose production yield and chemical and morphological structures from different tunicate species. Cellulose 21:3427–3441

    Article  CAS  Google Scholar 

  5. Troedsson C, Thompson E, Bouquet JM, Magnesen T, Schander C, Li J (2013) Tunicate extract for use in animal feeds.WO2013088177A1

  6. Zhao Y, Zhang Y, Lindström ME, Li J (2015) Tunicate cellulose nanocrystals: preparation, neat films and nanocomposite films with glucomannans. Carbohydr Polym 117:286–296

    Article  CAS  PubMed  Google Scholar 

  7. Bell JD, Barnard ML, Parkes HG, Thomas EL, Brennan CH, Cunnane SC, Dagnelie PC (1996) Effects of n-3 fatty acids on the NMR profile of plasma lipoproteins. J Lipid Res 37:1664–1674

    CAS  PubMed  Google Scholar 

  8. Fritsche K (2006) Fatty acids as modulators of the immune response. Annu Rev Nutr 26:45–73

    Article  CAS  PubMed  Google Scholar 

  9. Connor WE (2000) Importance of n-3 fatty acids in health and disease. Am J Clin Nutr 71:171S–175S

    CAS  PubMed  Google Scholar 

  10. Rizos EC, Ntzani EE, Bika E, Kostapanos MS, Elisaf MS (2012) Association between omega-3 fatty acid supplementation and risk of major cardiovascular disease events: a systematic review and meta-analysis. JAMA 308:1024–1033

    Article  CAS  PubMed  Google Scholar 

  11. Larsson SC, Kumlin M, Ingelman-Sundberg M, Wolk A (2004) Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 79:935–945

    CAS  PubMed  Google Scholar 

  12. Kris-Etherton PM, Grieger JA, Etherton TD (2009) Dietary reference intakes for DHA and EPA. Prostaglandins Leukot Essent Fatty Acids 81:99–104

    Article  CAS  PubMed  Google Scholar 

  13. Shahidi F, Wanasundara UN (1998) Omega-3 fatty acid concentrates: nutritional aspects and production technologies. Trends Food Sci Technol 9:230–240

    Article  CAS  Google Scholar 

  14. Xu B, Zhang X, Jin H, Wang C (2003) Determination of content of fat and composition of fatty acids in Ascidian. Chin J Mar Drugs 93(37–39):68

    Google Scholar 

  15. Zhang X, Jiang A, Wang C (2004) Extraction of fatty acid from Ciona intestinalis Linnaeus. Bull Mar Sci 23:93–96

    Google Scholar 

  16. Jiang A, Liu X, Wang C (2005) Extraction and antioxidant stability of ascidian oil. Mar Fish Res 26:32–37

    Google Scholar 

  17. Shi Y, Zheng Q, Mi B, Chen P, Xu B (2011) Analysis of nutritional components in Ciona intestinalis. J Anhui Agric Sci 39(12235–12236):12324

    Google Scholar 

  18. Puccia E, Messina CM, Cangialosi MV, D’Agati P, Mansueto C, Pellerito C, Nagy L, Mansueto V, Scopelliti M, Fiore T, Pellerito L (2005) Lipid and fatty acid variations in Ciona intestinalis ovary after tri-n-butyltin(IV)chloride exposure. Appl Organomet Chem 19:23–29

    Article  CAS  Google Scholar 

  19. Voogt PA, Van Rheenen JWA (1975) On the sterols of some ascidians. Arch Physiol Biochem 83:563–572

    CAS  Google Scholar 

  20. Gupta KC, Miller RL, Williams JR, Gagosian RB, Heinzer F (1979) Sterol Composition of Ciona intestinalis. J Nat Prod 42:305–306

    Article  Google Scholar 

  21. Ballantine JA, Lavis A, Roberts JC, Morris RJ (1977) Marine sterols. V. sterols of some Tunicata. The occurrence of saturated ring sterols in these filter-feeding organisms. J Exp Mar Biol Ecol 30:29–44

    Article  CAS  Google Scholar 

  22. Morris RJ, Mccartney MJ, Bone Q (1982) The distribution of sterols and stanols in the tunicate Ciona intestinalis. J Mar Biol Assoc UK 62:117–123

    Article  CAS  Google Scholar 

  23. Ito M, Yokoi K, Inoue T, Asano S, Hatano R, Shinohara R, Itonori S, Sugita M (2009) Sphingomyelins in four ascidians, Ciona intestinalis, Halocynthia roretzi, Halocynthia aurantium, and Styela clava. J Oleo Sci 58:473–480

    Article  CAS  PubMed  Google Scholar 

  24. Harumi T, Santis RD, Pinto MR, Suzuki N (1990) Phospholipid utilization in ascidian Ciona intestinalis spermatozoa during swimming. Comp Biochem Physiol A Physiol 96:263–265

    Article  Google Scholar 

  25. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  26. Nestor G, Bankefors J, Sandström C, Schlechtriem C, Pickova J, Brännäs E (2010) High-resolution 1 H magic angle spinning nmr spectroscopy of intact arctic char (Salvelinus alpinus) muscle. Quantitative analysis of n-3 fatty acids, EPA and DHA. J Agric Food Chem 58:10799–10803

    Article  CAS  PubMed  Google Scholar 

  27. Mahrous EA, Lee RB, Lee RE (2008) A rapid approach to lipid profiling of mycobacteria using 2D HSQC NMR maps. J Lipid Res 49:455–463

    Article  CAS  PubMed  Google Scholar 

  28. Nakamura MJ, Hotta K, Oka K (2013) Raman spectroscopic imaging of the whole Ciona intestinalis embryo during development. PLoS ONE 8:e71739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Pope EC, Rowley AF (2002) The heart of Ciona intestinalis: eicosanoid-generating capacity and the effects of precursor fatty acids and eicosanoids on heart rate. J Exp Biol 205:1577–1583

    CAS  PubMed  Google Scholar 

  30. Dagorn F, Dumay J, Wielgosz-Collin G, Rabesaotra V, Viau M, Monniot C, Biard J-F, Barnathan G (2010) Phospholipid distribution and phospholipid fatty acids of the tropical tunicates Eudistoma sp. and Leptoclinides uniorbis. Lipids 45:253–261

    Article  CAS  PubMed  Google Scholar 

  31. Viracaoundin I, Barnathan G, Gaydou EM, Aknin M (2003) Phospholipid FA from Indian Ocean tunicates Eudistoma bituminis and Cystodytes violatinctus. Lipids 38:85–88

    Article  CAS  PubMed  Google Scholar 

  32. Mayzaud P, Boutoute M, Perissinotto R, Nichols P (2007) Polar and neutral lipid composition in the pelagic tunicate Pyrosoma atlanticum. Lipids 42:647–657

    Article  CAS  PubMed  Google Scholar 

  33. Sargent JR, Whittle KJ (1981) Lipids and hydrocarbons in the marine food web. In: Longhurst AR (ed) Analysis of marine ecosystems. Academic Press, London

    Google Scholar 

  34. Nichols PD, Volkman JK, Johns RB (1983) Sterols and fatty acids of the marine unicellular alga, fcrg 51. Phytochemistry 22:1447–1452

    Article  CAS  Google Scholar 

  35. Yasuda S (1975) Sterol compositions of sea squirts (Ascidiacea). Comp Biochem Physiol B: Biochem Mol Biol 50:399–402

    CAS  Google Scholar 

  36. Schiller J, Zschornig O, Petkovic M, Muller M, Arnhold J, Arnold K (2001) Lipid analysis of human HDL and LDL by MALDI-TOF mass spectrometry and (31)P-NMR. J Lipid Res 42:1501–1508

    CAS  PubMed  Google Scholar 

  37. Köfeler HC, Fauland A, Rechberger GN, Trötzmüller M (2012) mass spectrometry based lipidomics: an overview of technological platforms. Metabolites 2:19–38

    Article  PubMed Central  PubMed  Google Scholar 

  38. Dong W, Shen Q, Baibado JT, Liang Y, Wang P, Huang Y, Zhang Z, Wang Y, Cheung H-Y (2013) Phospholipid analyses by MALDI-TOF/TOF mass spectrometry using 1,5-diaminonaphthalene as matrix. Int J Mass Spectrom 343–344:15–22

    Article  Google Scholar 

  39. Brugger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD (1997) Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci U S A 94:2339–2344

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Harvey DJ (1995) Matrix-assisted laser desorption/ionization mass spectrometry of sphingo- and glycosphingo-lipids. J Mass Spectrom 30:1311–1324

    Article  CAS  Google Scholar 

  41. Michalski MC, Genot C, Gayet C, Lopez C, Fine F, Joffre F, Vendeuvre JL, Bouvier J, Chardigny JM, Raynal-Ljutovac K (2013) Multiscale structures of lipids in foods as parameters affecting fatty acid bioavailability and lipid metabolism. Prog Lipid Res 52:354–373

    Article  CAS  PubMed  Google Scholar 

  42. Cansell M, Nacka F, Combe N (2003) Marine lipid-based liposomes increase in vivo FA bioavailability. Lipids 38:551–559

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The China Scholarship Council (CSC) and KTH are acknowledged for supporting Y. Zhao’s and M. Wang’s Ph.D. studies at KTH. J-M. Bouquet, T. Magnesen, E. M. Thompson and C. Troedsson from Bergen Norway are thanked for their help in sampling C. intestinalis specimens.

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Authors and Affiliations

  1. Department of Fibre and Polymer Technology, KTH Royal Institute of Technology, Teknikringen 56-58, 100 44, Stockholm, Sweden

    Yadong Zhao, Miao Wang, Mikael E. Lindström & Jiebing Li

Authors
  1. Yadong Zhao
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  2. Miao Wang
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Correspondence to Jiebing Li.

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Zhao, Y., Wang, M., Lindström, M.E. et al. Fatty Acid and Lipid Profiles with Emphasis on n-3 Fatty Acids and Phospholipids from Ciona intestinalis . Lipids 50, 1009–1027 (2015). https://doi.org/10.1007/s11745-015-4049-1

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  • DOI: https://doi.org/10.1007/s11745-015-4049-1

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