Journal of Applied Phycology

, Volume 17, Issue 4, pp 287–300

Lipid and fatty acid yield of nine stationary-phase microalgae: Applications and unusual C24–C28 polyunsaturated fatty acids

  • Maged P. Mansour
  • Dion M. F. Frampton
  • Peter D. Nichols
  • John K. Volkman
  • Susan I. Blackburn
Article

Abstract

Nine microalgal species from the classes Bacillariophyceae, Cryptophyceae, Prymnesiophyceae and Dinophyceae were isolated from Australian waters, cultured to stationary phase and analyzed for their lipid and fatty acid composition and yield. Five species (Pavlova pinguis, Heterocapsa niei, Proteomonas sulcata, Navicula jeffreyi and Thalassiosira pseudonana) produced high proportions of triacylglycerol (TAG: 22–57% total lipid). An unidentified Navicula-like diatom (CS-786), despite having a low TAG content, had the highest EPA yield (5.8 mg L−1), due to high biomass and a high relative proportion of EPA. Heterocapsa niei had the highest DHA yield (2.9 mg L−1), due to a high cellular lipid and DHA content (171 pg cell−1 and 13.7 pg cell−1, respectively) despite its relatively low biomass. The desirable PUFA composition and yield of both diatom CS-786 and H. niei make them potential candidates for optimization of biomass and PUFA production for use as live-feeds in aquaculture. In addition, H. niei may have potential as a source of DHA for other uses. Low proportions (< 1.2%) of 24:6(n−3) accompanied by trace proportions of 24:5(n−6) were detected in most strains, while 28:8(n−3) was found in dinoflagellates and also in the prymnesiophyte P. pinguis. All non-diatomaceous species contained 26:7(n−3) in minor quantities. This is the first time these unusual C24 and C26 PUFA have been reported in microalgae and the first report of C28 PUFA in a microalga other than dinoflagellates. Possible biosynthetic reasons why these might occur in stationary phase cultures are considered and the likely dietary transfer of these PUFA to higher aquatic life is discussed.

Keywords

C24 C26 C28 DHA EPA fatty acids lipid yield microalgae PUFA TAG triacylglycerols 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bazan NG, Colangelo V, Lukiw WJ (2002) Prostaglandins and other lipid mediators in Alzheimer’s disease. Prostaglandins & Other Lipid Mediators 68-69: 197–210.Google Scholar
  2. Blackburn SI, Bolch CJ, Haskard KA, Hallegraeff GM (2001) Reproductive compatibility among four global populations of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). Phycologia 40: 78–87.Google Scholar
  3. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 912–917.Google Scholar
  4. Bowles RD, Hunt AE, Bremer GB, Duchars MG, Eaton RA (1999) Long-chain n-3 polyunsaturated fatty acid production by the members of the marine protistan group the thraustochytrids: Screening of isolates and optimisation of docosahexaenoic acid production. J. Biotechnol. 70: 193–202.CrossRefGoogle Scholar
  5. Brown MR, Dunstan GA, Norwood SJ, Miller KA (1996) Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana. J. Phycol. 34: 64–73.CrossRefGoogle Scholar
  6. Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151: 315–331.CrossRefGoogle Scholar
  7. Carballeira NM, Sostre A, RodrÍguez AD (1997) Phospholipid fatty acid composition of gorgonians of the genus Eunicea: Further identification of tetracosapolyenoic acids. Comp. Biochem. Physiol. B 118: 257–260.CrossRefGoogle Scholar
  8. Carlson SE (1999) Long-chain polyunsaturated fatty acids and development of human infants. Acta-Paediatrica 88(Suppl. 430): 72–77.CrossRefPubMedGoogle Scholar
  9. Carvlalho AP, Malcata FX (2000) Effect of culture media on production of polyunsaturated fatty acids by Pavlova lutheri. Cryptogamie Algol. 21: 59–71.CrossRefGoogle Scholar
  10. Dunstan GA, Volkman JK, Barrett SM, Garland CD (1993) Changes in the lipid composition and maximisation of the polyunsaturated fatty acid content of three microalgae grown in mass culture. J. Appl. Phycol. 5: 71–83.Google Scholar
  11. Dunstan GA, Volkman JK, Barrett SM, Leroi J-M, Jeffrey SW (1994) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35: 155–161.CrossRefGoogle Scholar
  12. Dunstan GA, Volkman JK, Jeffrey SW, Barrett SM (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 2. Lipid classes and fatty acids. J. Exp. Mar. Biol. Ecol. 161: 115–134.CrossRefGoogle Scholar
  13. Enright CT, Newkirk GF, Craigie JS, Castell JD (1986) Growth of juvenile Ostrea edulis L. fed Chaetoceros calcitrans Schütt of varied chemical composition. J. Exp. Mar. Biol. Ecol. 96: 15–26.CrossRefGoogle Scholar
  14. Ghys A, Bakker E, Hornstra G, van den Hout M (2002) Red blood cell and plasma phospholipid arachidonic and docosahexaenoic acid levels at birth and cognitive development at 4 years of age. Early Human Development 69: 83–90.CrossRefPubMedGoogle Scholar
  15. Go JV, Řezanka T, Srebnik M, Dembitsky VM (2002) Variability of fatty acid components of marine and freshwater gastropod species from the littoral zone of the Red Sea, Mediterranean Sea, and Sea of Galilee. Biochem. Syst. Ecol. 30: 819–835.CrossRefGoogle Scholar
  16. Guillard RRL (1973) Division rates, in Stein Jr (ed), Handbook of Phycological Methods: Culture Methods and Growth Measurements, Cambridge University Press, Cambridge, pp. 289–311.Google Scholar
  17. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervaceaCleve. Can. J. Microbiol. 8: 229–239.PubMedGoogle Scholar
  18. Harrison PJ, Thompson PA, Calderwood GS (1990) Effects of nutrient and light limitation on the biochemical composition of phytoplankton. J. Appl. Phycol. 2: 45–56.Google Scholar
  19. Kawasaki K, Nabeshima YI, Ishihara K, Kaneniwa M, Ooizumi T (2000) High level of 6,9,12,15,18,21-tetracosahexaenoic acid found in lipids of Ophiuroidea Ophiura sarsi Lütken. Fish. Sci. 66: 614–615.CrossRefGoogle Scholar
  20. Kubota T, Tsuda M, Kobayashi J (2000) Amphodinolide V, novel 14-membered macrolide from marine dinoflagellate Amphidinium sp. Tetrahedron Lett. 41(5): 713–716.CrossRefGoogle Scholar
  21. Leblond JD, Chapman PJ (2000) Lipid class distribution of highly unsaturated long chain fatty acids in marine dinoflagellates. J. Phycol. 36: 1103–1108.CrossRefGoogle Scholar
  22. Lewis T, Nichols PD, McMeekin TA (2000) Evaluation of extraction methods for recovery of fatty acids from lipid-producing microheterotrophs. J. Microbiol. Methods 43: 107–116.CrossRefPubMedGoogle Scholar
  23. McKenzie JD, Black KD, Kelly MS, Newton LC, Handley LL, Scrimgeour CM, Raven JA, Henderson RJ (2000) Comparisons of fatty acid and stable isotope ratios in symbiotic and non-symbiotic brittlestars from Oban Bay, Scotland. J. Mar. Biol. Ass. U.K. 80: 311–320.CrossRefGoogle Scholar
  24. McKinnon AD, Duggan S, Nichols PD, Rimmer MA, Semmens G, Robino B (2003) The potential of tropical paracalanid copepods as live feeds in aquaculture. Aquaculture 223: 89–106.CrossRefGoogle Scholar
  25. Makrides M, Neumann M, Simmer K, Pater J, Gibson R (1995) Are long‐chain polyunsaturated fatty acids essential nutrients in infancy? The Lancet 345: 1463–1468.CrossRefGoogle Scholar
  26. Mansour MP, Volkman JK, Holdsworth DG, Jackson AE, Blackburn SI (1999a) Very-long-chain (C28) highly unsaturated fatty acids in marine dinoflagellates. Phytochemistry 50: 541–548.CrossRefGoogle Scholar
  27. Mansour MP, Volkman JK, Jackson AE, Blackburn SI (1999b) The fatty acid and sterol composition of five marine dinoflagellates. J. Phycol. 35: 710–720.CrossRefGoogle Scholar
  28. Mansour MP, Volkman JK, Blackburn SI (2003) The effect of growth phase on the lipid, fatty acid and sterol composition in the marine dinoflagellate, Gymnodinium sp. in batch culture. Phytochemistry 63: 145–153.CrossRefPubMedGoogle Scholar
  29. Mansour MP, Holdsworth DG, Forbes S, Macleod C, Volkman JK (2005) High contents of 24:6(n-3) and 20:1(n-13) fatty acids in the brittle star Amphiura elandiformis from Tasmanian coastal sediments. Biochem. Syst. Ecol. 33: 659–674.CrossRefGoogle Scholar
  30. Martínez-Fernández E, Acosta-Salmón H, Rangel-Dávalos C (2004) Ingestion and digestion of 10 species of microalgae by winged pearl oyster Pteria sterna (Gould, 1851) larvae. Aquaculture 230: 417–423.CrossRefGoogle Scholar
  31. Myers RA, Worm B (2003) Rapid world wide depletion of predatory fish communities. Nature 423: 280–283.CrossRefPubMedGoogle Scholar
  32. Nichols PD, Danaher KT, Koslow JA (2003) Occurrence of high levels of tetracosahexaenoic acid in the jellyfish Aurelia sp. Lipids 38: 1207–1210.PubMedGoogle Scholar
  33. Nichols BW, Harris P, James AT (1965) The biosynthesis of trans3-hexadecenoic acid by Chlorella vulgaris. Biochem. Biophys. Res. Commun. 21: 473–79.CrossRefPubMedGoogle Scholar
  34. Ota T, Chihara Y, Itabashi Y, Takagi T (1994a) Occurrence of all-cis-6,9,12,15,18,21-tetracosahexaenoic acid in flatfish lipids. Fish. Sci. 60: 171–175.Google Scholar
  35. Ota T, Kawabata Y, Ando Y (1994b) Positional distribution of 24:6(n-3) in triacyl-sn-glycerols from flathead flounder liver and flesh. J. Amer. Oil Chem. Soc. 71: 475–478.Google Scholar
  36. Peet M, Brind J, Ramchand CN, Shah S, Vankar GK (2001) Two double-blind placebo-controlled pilot studies of eicosapentaenoic acid in the treatment of schizophrenia. Schizophrenia Res. 49: 243–251.CrossRefGoogle Scholar
  37. Phleger CF, Nelson MM, Mooney BD, Nichols PD (2001) Interannual variations in the lipids of the Antarctic pteropods Clione limacine and Clio pyramidata. Comp. Biochem. Physiol. B 128: 553–564.CrossRefPubMedGoogle Scholar
  38. Rashida A, Karmali JD (1996) Historical perspective and potential use of n-3 fatty acids in therapy of cancer cachexia. Suppl. Nutrit. 12: S2–S4.Google Scholar
  39. Reitan KI, Rainuzzo JR, Oie G, Olsen Y (1997) A review of the nutritional effects of algae in marine fish larvae. Aquaculture 155: 207–221.CrossRefGoogle Scholar
  40. Renaud SM, Thinh L-V, Parry DL (1999) The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 170: 147–159.CrossRefGoogle Scholar
  41. Řezanka T (2000) Analysis of very long chain polyunsaturated fatty acids using high-performance liquid chromatography – atmospheric pressure chemical ionization mass spectrometry. Biochem. Syst. Ecol. 28: 847–856.CrossRefPubMedGoogle Scholar
  42. Rose DP, Connolly JM (1999) Omega-3 fatty acids as cancer chemopreventative agents. Pharmacology &Therapeutics 83: 217–244.Google Scholar
  43. Sato D, Ando Y, Tsujimoto R, Kawasaki K-I (2001) Identification of novel nonmethylene-interrupted fatty acids, 7E,13E-20:2, 7E,13E,17Z-20:3, 9E,15E,19Z-22:3, and 4Z,9E,15E,19Z-22:4, in Ophiuroidea (brittle star) lipids. Lipids 36: 1371–1375.PubMedGoogle Scholar
  44. Sherr EB, Sherr BF (1993) Preservation and storage of samples for enumeration of heterotrophic protists, in Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Florida, pp. 207–212.Google Scholar
  45. Shifrin NS, Chisholm SW (1981) Phytoplankton lipids: Interspecific differences and effects of nitrate, silicate and light-dark cycles. J. Phycol. 17: 374–384.CrossRefGoogle Scholar
  46. Sidhu KS (2003) Health benefits and potential risks related to consumption of fish or fish oil. Regul. Toxicol. Pharmacol. 38: 336–344.CrossRefPubMedGoogle Scholar
  47. Stevens LJ, Zentall SS, Abate ML, Kuczek T, Burgess JR (1996) Omega-3 fatty acids in boys with behavior, learning, and health problems. Physiology &Behavior 59: 915–920.Google Scholar
  48. Su K-P, Shen WW, Huang S-Y (2001) Omega-3 fatty acids as a psychotherapeutic agent for a pregnant schizophrenic patient. Eur. Neuropsychopharmacol. 11: 295–299.CrossRefPubMedGoogle Scholar
  49. Svetashev VI, Vysotskii MV (1998) Fatty acids of Heliopora coerulea and chemotaxonomic significance of tetracosapolyenoic acids in coelenterates. Comp. Biochem. Physiol. B 119: 73–75.CrossRefGoogle Scholar
  50. Takagi T, Kaneniwa M, Itabashi Y (1986) Fatty acids in Crinoidea and Ophiuroidea – Occurrence of all-cis-6,9,12,15,18,21-tetracosahexaenoic acid. Lipids 21: 430–433.Google Scholar
  51. Thomas WH, Seibert DLR, Alden M, Neori A, Eldridge P (1984) Yields, photosynthetic efficiencies and proximate composition of dense marine microalgal cultures. III. Isochrysis sp. and Monallantus salina experiments and comparative conclusions. Biomass 5: 299–316.CrossRefGoogle Scholar
  52. Tonon T, Harvey D, Larson TR, Graham IA (2002) Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae. Phytochemistry 61: 14–24.CrossRefGoogle Scholar
  53. Tredici MR (1999) Bioreactors, Photo, in Flickinger MC, Drew SW (eds), Encyclopedia of Bioprocess Technology: Fermentation, Biocataylsis, and Bioseparation, Wiley, NY, pp. 395–419.Google Scholar
  54. Van Pelt CK, Huang M-C, Tschanz CL, Brenna JT (1999) An octaene fatty acid, 4,7,10,13,16,19,22,25-octacosaoctaenoic acid (28: 8n-3), found in marine oils. J. Lipid Res. 40: 1501–1505.PubMedGoogle Scholar
  55. Volkman JK, Jeffrey SW, Nichols PD, Rogers GI, Garland CD (1989) Fatty acids and lipids of ten species of microalgae used in mariculture. J. Exp. Mar. Biol. Ecol. 128: 219–240.CrossRefGoogle Scholar
  56. Volkman JK, Nichols PD (1991) Applications of thin layer chromatography-flame ionization detection to the analysis of lipids and pollutants in marine and environmental samples. J. Planar Chromatogr. 4: 19–26.Google Scholar
  57. Vysotskii MV, Svetashev VI (1991) Identification, isolation and characterization of tetracosapolyenoic acids in lipids of marine coelenterates. Biochim. Biophys. Acta 1083: 161–165.PubMedGoogle Scholar
  58. Wroble M, Mash C, Williams L, McCall RB (2002) Should long chain polyunsaturated fatty acids be added to infant formula to promote development? Appl. Develop. Psychol. 23: 99–112.CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Maged P. Mansour
    • 1
  • Dion M. F. Frampton
    • 1
  • Peter D. Nichols
    • 1
  • John K. Volkman
    • 1
  • Susan I. Blackburn
    • 1
  1. 1.CSIRO Marine ResearchHobartAustralia

Personalised recommendations