LC-PUFA-enriched oil production by microalgae: Accumulation of lipid and triacylglycerols containing n-3 LC-PUFA is triggered by nitrogen limitation and inorganic carbon availability in the marine haptophyte Pavlova lutheri

Marine Drugs

Volumn 11, Issue 11, 2013, Pages 4246-4266

  Guihéneuf, Freddy ^a   Stengel, Dagmar B ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Microalgae; n 3 LC PUFA; Pavlova lutheri; Sodium bicarbonate; Triacylglycerol

Indexed keywords

BICARBONATE; CARBON; NITROGEN; OIL; OMEGA 3 FATTY ACID; POLYUNSATURATED FATTY ACID; TRIACYLGLYCEROL;

ALKALINITY; ARTICLE; CELL STRESS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HAPTOPHYTA; LIPID STORAGE; MICROALGA; NONHUMAN; PAVLOVA LUTHERI; PH;

PAVLOVA LUTHERI;

CARBON; FATTY ACIDS; FATTY ACIDS, OMEGA-3; FISH OILS; HAPTOPHYTA; HYDROGEN-ION CONCENTRATION; LIPIDS; MICROALGAE; NITROGEN; SODIUM BICARBONATE; TRIGLYCERIDES;

EID: 84889255060     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md11114246     Document Type: Article

References (71)

1. Mata, T.M.; Martins, A.A.; Caetano, N.S. Microalgae for biodiesel production and other applications: A review. Renew. Sust. Energ. Rev. 2010, 14, 217-232.
2. Mimouni, V.; Ulmann, L.; Pasquet, V.; Mathieu, M.; Picot, L.; Bougaran, G.; Cadoret, J.P.; Morant-Manceau, A.; Schoefs, B. The potential of microalgae for the production of bioactive molecules of pharmaceutical interest. Curr. Pharm. Biotechnol. 2013, 13, 2733-2750.
3. Simopoulos, A.P. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 2002, 56, 365-379.
4. Simopoulos, A.P. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp. Biol. Med. 2008, 233, 674-688.
5. Worm, B.; Hilborn, R.; Baum, J.K.; Branch, T.A.; Collie, J.S.; Costello, C.; Fogarty, M.J.; Fulton, E.A.; Hutchings, J.A.; Jennings, S.; et al. Rebuilding global fisheries. Science 2009, 325, 578-585.
6. Khozin-Goldberg, I.; Iskandarov, U.; Cohen, Z. LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology. Appl. Microbiol. Biotechnol. 2011, 91, 905-915.
7. Martins, D.A.; Custódio, L.; Barreira, L.; Pereira, H.; Ben-Hamadou, R.; Varela, J.; Abu-Salah, K.M. Alternative sources of n-3 long-chain polyunsaturated fatty acids in marine microalgae. Mar. Drugs 2013, 11, 2259-2281
8. Berge, J.P.; Gouygou, J.P.; Dubacq, J.P.; Durand, P. Reassessment of lipid composition of the diatom, Skeletonema costatum. Phytochemistry 1995, 39, 1017-1021.
9. Alonso, D.L.; Belarbi, E.H.; Rodriguez-Ruiz, J.; Segura, C.I.; Gimenez, A. Acyl lipids of three microalgae. Phytochemistry 1998, 47, 1473-1483.
10. Tonon, T.; Harvey, D.; Larson, T.R.; Graham, I.A. Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae. Phytochemistry 2002, 61, 15-24.
11. Guihéneuf, F.; Fouqueray, M.; Mimouni, V.; Ulmann, L.; Jacquette, B.; Tremblin, G. Effect of UV stress on the fatty acid and lipid class composition in two marine microalgae Pavlova lutheri (Pavlovophyceae) and Odontella aurita (Bacillariophyceae). J. Appl. Phycol. 2010, 22, 629-638.
12. Meireles, L.A.; Guedes, A.C.; Malcata, F.X. Lipid class composition of the microalga Pavlova lutheri: eicosapentaenoic and docosahexaenoic acids. J. Agric. Food Chem. 2003, 51, 2237-2241.
13. Bigogno, C.; Khozin-Goldberg, I.; Boussiba, S.; Vonshak, A.; Cohen, Z. Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 2002, 5, 497-503.
14. Khozin-Goldberg, I.; Bigogno, C.; Shrestha, P.; Cohen, Z. Nitrogen starvation induces the accumulation of arachidonic acid in the freshwater green alga Parietochloris incisa (Trebouxiophyceae). J. Phycol. 2002, 38, 991-994.
15. Yu, E.T.; Zendejas, F.J.; Lane, P.D.; Gaucher, S.; Simmons, B.A.; Lane, T.W. Triacylglycerol accumulation and profiling in the model diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum (Baccilariophyceae) during starvation. J. Appl. Phycol. 2009, 21, 669-681.
16. Roessler, P.G. Effects of silicon deficiency on lipid composition and metabolism in the diatom Cyclotella cryptica. J. Phycol. 1988, 24, 394-400.
17. Khozing-Goldberg, I.; Cohen, Z. The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 2006, 67, 696-701.
18. Gong, Y.; Guo, X.; Wan, X.; Liang, Z.; Jiang, M. Triacylglycerol accumulation and change in fatty acid content of four marine oleaginous microalgae under nutrient limitation and at different culture ages. J. Basic Microb. 2013, 53, 29-36.
19. Hu, Q.; Sommerfeld, M.; Jarvis, E.; Ghirardi, M.; Posewitz, M.; Seibert, M.; Darzins, A. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 2008, 54, 621-639.
20. Breuer, G.; Lamers, P.P.; Martens, D.E.; Wijffels, R.H. The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour. Technol. 2012, 124, 217-226.
21. Mortensen, S.H.; Borsheim, K.Y.; Rainuzzo, J.; Knutsen, G. Fatty acid and elemental composition of the marine diatom Chaetoceros gracilis Schutt. Effects of silicate deprivation, temperature and light intensity. J. Exp. Mar. Biol. Ecol. 1988, 122, 173-185.
22. Pal, D.; Khozin-Goldberg, I.; Cohen, Z.; Boussiba, S. The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl. Microbiol. Biotechnol. 2011, 90, 1429-1441.
23. Fidalgo, J.P.; Cid, A.; Torres, E.; Sukenik, A.; Herrero, C. Effects of nitrogen source and growth phase on proximate biochemical composition, lipid classes and fatty acid profile of the marine microalga Isochrysis galbana. Aquaculture 1998, 166, 105-116.
24. Roncarati, A.; Meluzzi, A.; Acciarri, S.; Tallarico, N.; Meloti, P. Fatty acid composition of different microalgae strains (Nannochloropsis sp., Nannochloropsis oculata (Droop) Hibberd, Nannochloris atomus Butcher and Isochrysis sp.) according to the culture phase and the carbon dioxide concentration. J. World Aquacult. Soc. 2004, 35, 401-411.
25. Illman, A.L.; Scragg, A.H.; Shales, S.W. Increase in Chlorella strains calorific values when grown in low nitrogen medium. Enzyme Microb. Tech. 2000, 27, 631-635.
26. Hsieh, C.-H.; Wu, W.-T. Cultivation of microalgae for oil production with a cultivation strategy of urea limitation. Bioresour. Technol. 2009, 100, 3921-3926.
27. Griffiths, M.J.; van Hille, R.P.; Harrison, S.T.L. Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. J. Appl. Phycol. 2012, 24, 989-1001.
28. Kaplan, D.; Richmond, A.E.; Dubinsky, Z.; Aaronson, S. Algal nutrition. In Handbook of Microalgal Mass Culture; Richmond, A., Ed.; CRC Press: Boca Raton, FL, USA, 1986; pp. 147-198.
29. 2 concentration during growth on fatty acid composition in microalgae. Plant Physiol. 1990, 93, 851-856.
30. 2 and nitrogen supply on lipid class composition of Dunaliella viridis. J. Appl. Phycol. 1998, 10, 135-144.
31. 2 concentration. Biotechnol. Lett. 2006, 28, 987-992.
32. 2 and light intensity under batch and continuous cultivation modes. Mar. Biotechnol. 2005, 7, 381-388.
33. 2 aeration. Bioresour. Technol. 2009, 100, 833-838.
34. Tang, H.; Abunasser, N.; Garcia, M.E.D.; Chen, M.; Simon Ng, K.Y.; Salley, S.O. Potential of microalgae oil from Dunaliella tertiolecta as a feedstock for biodiesel. Appl. Energ. 2011, 88, 3324-330.
35. Hsueh, H.T.; Chu, H.; Yu, S.T. A batch study on the bio-fixation of carbon dioxide in the absorbed solution from a chemical wet scrubber by hot spring and marine algae. Chemosphere 2007, 66, 878-886.
36. Guihéneuf, F.; Mimouni, V.; Ulmann, L.; Tremblin, G. Combined effects of irradiance level and carbon source on fatty acid and lipid class composition in the microalga Pavlova lutheri commonly used in mariculture. J. Exp. Mar. Biol. Ecol. 2009, 369, 136-143.
37. Gardner, R.D.; Cooksey, K.E.; Mus, F.; Macur, R.; Moll, K.; Eustance, E.; Carlson, R.P.; Gerlach, R.; Fields, M.W.; Peyton, B.M. Use of sodium bicarbonate to stimulate triacylglycerol accumulation in the chlorophyte Scenedesmus sp. and the diatom Phaeodactylum tricornutum. J. Appl. Phycol. 2012, 24 1311-1320.
38. 2 and bicarbonate as inorganic carbon sources for triacylglycerol and starch accumulation in Chlamydomonas reinhardtii. Biotechnol. Bioeng. 2013, 110, 87-96.
39. White, D.A.; Pagarette, A.; Rooks, P.; Ali, S.T. The effect of sodium bicarbonate supplementation on growth and biochemical composition of marine microalgae cultures. J. Appl. Phycol. 2013, 25, 153-165.
40. Mus, F.; Toussaint, J.-P.; Cooksey, K.E.; Fields, M.W.; Gerlach, R.; Peyton, B.M.; Carlson, R.P. Physiological and molecular analysis of carbon source supplementation and pH stress-induced lipid accumulation in the marine diatom Phaeodactylum tricornutum. Appl. Microbiol. Biotechnol. 2013, 97, 3625-3642.
41. Peng, X.; Liu, S.; Zhang, W.; Zhao, Y.; Chen, L.; Wang, H.; Liu, T. Triacylglycerol accumulation of Phaeodactylum tricornutum with different supply of inorganic carbon. J. Appl. Phycol. 2013, in press.
42. Guckert, J.; Cooksey, K. Triglyceride accumulation and fatty acid profile changes in Chlorella (Chlorophyta) during high pH-induced cell inhibition. J. Phycol. 1990, 26, 72-79.
43. Gardner, R.; Peters, P.; Peyton, B.; Cooksey, K. Medium pH and nitrate concentration effects on accumulation of triacylglycerol in two members of the Chlorophyta. J. Appl. Phycol. 2011, 26, 1005-1016.
44. Toledo-Cervantes, A.; Morales, M.; Novelo, E.; Revah, S. Carbon dioxide fixation and lipid storage by Scenedesmus obtusiusculus. Bioresour. Technol. 2013, 130, 152-158.
45. Jiang, Y.; Yoshida, T.; Quigg, A. Photosynthetic performance, lipid production and biomass composition in response to nitrogen limitation in marine microalgae. Plant Physiol. Biotechnol. 2012, 54, 70-77.
46. Guedes, A.C.; Meireles, L.A.; Amaro, H.M.; Malcata, F.X. Changes in lipid class and fatty acid composition of cultures of Pavlova lutheri, in response to light intensity. J. Am. Oil Chem. Soc. 2010, 87, 791-801.
47. Guihéneuf, F.; Ulmann, L.; Tremblin, G.; Mimouni, V. Light-dependent utilization of two radiolabelled carbon sources, sodium bicarbonate and sodium acetate, and relationships with long chain polyunsaturated fatty acid synthesis in the microalga Pavlova lutheri (Haptophyta). Eur. J. Phycol. 2011, 46, 143-152.
48. Nimer, N.A.; Iglesias-Rodriguez, M.D.; Mmett, M.J. Bicarbonate utilization by marine phytoplankton species. J. Phycol. 1997, 33, 625-631.
49. Tremblin, G.; Robert, J.M. Carbon fixation by the peculiar marine diatom Haslea ostrearia. Photosynthetica 2001, 39, 215-220.
50. Rech, M.; Morant-Manceau, A.; Tremblin, G. Carbon fixation and carbonic anhydrase activity in Haslea ostrearia (Bacillariophyceae) in relation to growth irradiance. Photosynthetica 2008, 46, 52-62.
51. Reinfelder, J.R. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu. Rev. Mar. Sci. 2011, 3, 291-315.
52. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 2005, 56, 99-131.
53. Chen, C.Y.; Durbin, E.G. Effects of pH on the growth and carbon uptake of marine phytoplankton. Mar. Ecol. Prog. Ser. 1994, 109, 83-94.
54. Guihéneuf, F.; Leu, S.; Zarka, A.; Khozin-Goldberg, I.; Khalilov, I.; Boussiba, S. Cloning and molecular characterization of a novel acyl-CoA:diacylglycerol acyltransferase 1-like gene (PtDGAT1) from the diatom Phaeodactylum tricornutum. FEBS J. 2011, 278, 3651-3666.
55. Recht, L.; Zarka, A.; Boussiba, S. Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Appl. Microbiol. Biotechnol. 2012, 94, 1495-1503.
56. Sukenik, A.; Yamaguchi, Y. Alterations in lipid molecular species of the marine eustigmatophyte Nannochloropsis sp. J. Phycol. 1993, 29, 620-626.
57. Brown, M.R.; Dunstan, G.A.; Norwood, S.J.; Miller, K.A. Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana. J. Phycol. 1996, 32, 64-73.
58. Tonon, T.; Harvey, D.; Larson, T.R.; Graham, I.A. Identification of a very long chain polyunsaturated fatty acid [Delta]4-desaturase from the microalga Pavlova lutheri. FEBS Lett. 2003, 553, 440-444.
59. Fan, J.; Yan, C.; Andre, C.; Shanklin, J.; Schwender, J.; Xu, C. Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol. 2012, 53, 1380-1390.
60. Ramanan, R.; Kim, B.-K.; Cho, D.-H.; Ko, S.-R.; Oh, H.-M.; Kim, H.-S. Lipid droplet synthesis is limited by acetate availability in starchless mutant of Chlamydomonas reinhardtii. FEBS Lett. 2013, 587, 370-377.
61. Cooksey, K.E.; Guckert, J.B.; Williams, S.A.; Callis, P.R. Fluorometric determination of the neutral lipid content of microalgal cells using Nile Red. J. Microbiol. Methods 1987, 6, 333-345.
62. Lee, S.; Yoon, B.-D.; Oh, H.-M. Rapid method for the determination of lipid from the green alga Botryococcus braunii. Biotechnol. Tech. 1998, 12, 553-556.
63. Chen, W.; Zhang, C.W.; Song, L.R.; Sommerfeld, M.; Hu, Q. A high throughput Nile Red method for quantitative measurement of neutral lipids in microalgae. J. Microbiol. Methods 2009, 77, 41-47.
64. Tatsuzawa, H.; Takizawa, E.; Changes in lipid and fatty acid composition of Pavlova lutheri. Phytochemistry 1995, 40, 397-400.
65. Culture Collection of Algae and Protozoa. Available online: http://www.ccap.ac.uk/ (accessed on 11 September 2013).
66. Guillard, R.R.L. Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrate Animals; Smith, W.L., Chanley, M.H., Eds.; Plenum Press: New York, NY, USA, 1975; pp. 29-60.
67. H2Ocean Salt Analysis. Available online: http://www.theaquariumsolution. com/files/H2Ocean %20Salt%20Analysis%20update-3.pdf (accessed on 11 September 2013).
68. Collos, Y.; Mornet, F.; Sciandra, A.; Waser, N.; Larson, A.; Harrison, P.J. An optical method for the rapid measurement of micromolar concentrations of nitrate in marine phytoplankton cultures. J. Appl. Phycol. 1999, 11, 179-184.
69. Greenspan, P.; Mayer, E.P.; Fowler, S.D. Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 1985, 100, 965-973.
70. Bligh, E.G.; Dyer, W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37, 911-917.
71. Li, Y.; Han, D.; Hu, G.; Dauvillee, D.; Sommerfeld, M.; Ball, S.; Hu, Q. Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab. Eng. 2010, 12, 387-391.