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Journal of Applied Phycology

, Volume 28, Issue 4, pp 2167–2175 | Cite as

Neutral lipid production in Dunaliella salina during osmotic stress and adaptation

  • Shuo Yao
  • Jingquan Lu
  • Zsuzsa Sárossy
  • Claus Baggesen
  • Anders Brandt
  • Yingfeng An
Article

Abstract

The salt-tolerant green microalga Dunaliella salina can survive both hyper- and hypo-osmotic shock. Upon osmotic shock, the cells transiently and rapidly decreased or increased in size within minutes and slowly over hours acquired their original cell size and volume. Cell size distribution differs significantly in the cultures grown in the salinity range from 1.5 to 15 % NaCl. By using Nile Red fluorescence to detect neutral lipids, it became clear that only hyper-osmotic shock on cells induced transient neutral lipid appearance in D. salina, while those transferred from 9 to 15 % NaCl stimulated the most neutral lipid accumulation. These cells grew well in 9 % NaCl, but they cannot recover a shift to 15 % NaCl and cell division is accordingly slowed down. The transient appearance of neutral lipid could be dependent on the inhibition of cell division experiencing the NaCl shift. Moreover, the effect of nutrient limitation slows down cell division and photosynthesis as a secondary result, which triggers the cells to accumulate neutral storage lipids when they entered the stationary phase, which is seen in all the batch cultures of D. salina grown in the salinity range of 3–15 %. The changes in salt concentration did not significantly influence the overall fatty acid composition in D. salina cells. Although there shows both increased amounts of total lipids and neutral lipids in the cells grown in salinity higher than 9 % NaCl, lipid productivity is however compromised by the slower cell growth rate and lower cell density under this condition.

Keywords

Dunaliella salina Neutral lipids Osmotic stress Salt adaptation Nutrient starvation 

Notes

Acknowledgments

This work was supported by Technical University of Denmark and Program for Excellent Talents in Shenyang Agricultural University. We thank Anne Olsen and Sannie Herleen Larsen for their technical support of this work.

References

  1. Avron M (1992) Osmoregulation. In: Avron M, Ben-Amotz A (eds) Dunaliella: physiology, biochemistry and biotechnology. CRC Press, Boca Raton, Florida, pp 135–164Google Scholar
  2. Avron A, Ben-Amotz A (1992) Dunaliella: physiology, biochemistry and biotechnology. CRC Press Boca-Raton, FloridaGoogle Scholar
  3. Ben-Amotz A, Lers A, Avron M (1988) Stereoisomers of β-carotene and phytoene in the alga Dunaliella bardawil. Plant Physiol 86:1286–1291CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ben-Amotz A, Shaish A, Avron M (1989) Mode of action of the massively accumulated β-carotene of Dunaliella bardawil in protecting the alga against damage by excess irradiation. Plant Physiol 91:1040–1043CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917CrossRefGoogle Scholar
  6. Borowitzka LJ, Brown AD (1974) The salt relations of marine and halophilic species of the uni cellular green alga Dunaliella the role of glycerol as a compatible solute. Arch Microbiol 96:37–52CrossRefGoogle Scholar
  7. Chapin FS (1991) Integrated responses of plants to stress. BioScience 41:29–36CrossRefGoogle Scholar
  8. Chen H, Jiang J (2009) Osmotic responses of Dunaliella to the changes of salinity. J Cell Physiol 219:251–258CrossRefPubMedGoogle Scholar
  9. Chen H, Jiang J, Wu G (2009) Effects of salinity changes on the growth of Dunaliella salina and its isozyme activities of glycerol-3-phosphate dehydrogenase. J Agric Food Chem 57:6178–6182CrossRefPubMedGoogle Scholar
  10. Chen M, Tang H, Ma H, Holland TC, Ng KY, Salley SO (2011) Effect of nutrients on growth and lipid accumulation in the green algae Dunaliella tertiolecta. Bioresour Technol 102:1649–1655CrossRefPubMedGoogle Scholar
  11. Davidi L, Katz A, Pick U (2012) Characterization of major lipid droplet proteins from Dunaliella. Planta 236:19–33CrossRefPubMedGoogle Scholar
  12. Davidi L, Shimoni E, Khozin-Goldberg I, Zamir A, Pick U (2014) Origin of β-carotene-rich plastoglobuli in Dunaliella bardawil. Plant Physiol 164:2139–2156CrossRefPubMedPubMedCentralGoogle Scholar
  13. Farese RV Jr, Walther TC (2009) Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139:855–860CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fisher M, Pick U, Zamir A (1994) A salt-induced 60 kilodalton plasma membrane protein plays a potential role in the extreme halotolerance of the alga Dunaliella. Plant Physiol 106:1359–1365PubMedPubMedCentralGoogle Scholar
  15. Hasegawa PM, Bressan RA, Zhu J, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499CrossRefPubMedGoogle Scholar
  16. Huang AH (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol 43:177–200CrossRefGoogle Scholar
  17. Jiang Y, Yoshida T, Quigg A (2012) Photosynthetic performance, lipid production and biomass composition in response to nitrogen limitation in marine microalgae. Plant Physiol Biochem 54:70–77CrossRefPubMedGoogle Scholar
  18. Lu C, Hills MJ (2002) Arabidopsis mutants deficient in diacylglycerol acyltransferase display increased sensitivity to abscisic acid, sugars, and osmotic stress during germination and seedling development. Plant Physiol 129:1352–1358CrossRefPubMedPubMedCentralGoogle Scholar
  19. Maeda M, Thompson GAJ (1986) On the mechanism of rapid plasma membrane and chloroplast envelope expansion in Dunaliella salina exposed to hypoosmoticshock. J Cell Biol 102:289–297CrossRefPubMedGoogle Scholar
  20. Peeler TC, Stephenson MB, Einspahr KJ, Thompson GA (1989) Lipid characterization of an enriched plasma membrane fraction of Dunaliella salina grown in media of varying salinity. Plant Physiol 89:970–976CrossRefPubMedPubMedCentralGoogle Scholar
  21. Pinkart HC, Devereux R, Chapman PJ (1998) Rapid separation of microbial lipids using solid phase extraction columns. J Microb Meth 34:9–15CrossRefGoogle Scholar
  22. Rogelio RS, Black M (1994) Osmotic potential and abscisic acid regulate triacylglycerol synthesis in developing wheat embryos. Planta 192:9–15Google Scholar
  23. Sadka A, Himmelhoch S, Zamir A (1991) A 150 Kilodalton cell surface protein is induced by salt in the halotolerant green alga Dunaliella salina. Plant Physiol 95:822–831CrossRefPubMedPubMedCentralGoogle Scholar
  24. Schwartz A, Sugg H, Ritter TW, Fernandez-Repollet E (1983) Direct determination of cell diameter, surface area, and volume with an electronic volume sensing flow cytometer. Cytometry 3:456–458CrossRefPubMedGoogle Scholar
  25. Shifrin NS, Chisholm SW (1981) Phytoplankton lipids: inter specific differences and effects of nitrate, silicate and light-dark cycles. J Phycol 17:374–384CrossRefGoogle Scholar
  26. Takagi M, Karseno YT (2006) Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J Biosci Bioeng 101:223–226CrossRefPubMedGoogle Scholar
  27. Teodoresco EC (1905) Organisation et développement du Dunaliella, nouveau genre de Volvocacée - Polyblépharidée. Bot Zentralbl Beih 18:215–232Google Scholar
  28. Thompson GA Jr (1996) Lipids and membrane function in green algae. Biochim Biophys Acta 1302:17–45CrossRefPubMedGoogle Scholar
  29. Weselake RJ, Pomeroy MK, Furukawa TL, Golden JL, Little DB, Laroche A (1993) Developmental profile of diacylglycerol acyltransferase in maturing seeds of oilseed rape and safflower and microspore-derived cultures of oilseed rape. Plant Physiol 102:565–571PubMedPubMedCentralGoogle Scholar
  30. Xu XQ, Berdall J (1997) Effect of salinity on fatty acid composition of a green microalga from an Antarctic hyper-saline lake. Phytochemistry 45:655–658CrossRefGoogle Scholar
  31. Yao S, Brandt A, Egsgaard H, Gjermansen C (2012) Neutral lipid accumulation at elevated temperature in conditional mutants of two microalgae species. Plant Physiol Biochem 61:71–79CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Shuo Yao
    • 1
  • Jingquan Lu
    • 2
  • Zsuzsa Sárossy
    • 2
  • Claus Baggesen
    • 2
  • Anders Brandt
    • 2
  • Yingfeng An
    • 1
  1. 1.College of Biological Science and TechnologyShenyang Agricultural UniversityShenyangChina
  2. 2.Department of Chemical and Biochemical Engineering, Risoe CampusTechnical University of DenmarkRoskildeDenmark

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