Journal of Applied Phycology

, Volume 27, Issue 4, pp 1425–1431 | Cite as

Selecting microalgae with high lipid productivity and photosynthetic activity under nitrogen starvation

  • Giulia Benvenuti
  • Rouke Bosma
  • María Cuaresma
  • Marcel Janssen
  • Maria J. Barbosa
  • René H. Wijffels


An economically feasible microalgal lipid industry heavily relies on the selection of suitable strains. Because microalgae lipid content increases under a range of adverse conditions (e.g. nutrient deprivation, high light intensity), photosynthetic activity is usually strongly reduced. As a consequence, lipid productivity rapidly declines overtime, after reaching a maximum within the first days of cultivation. The microalgae Chlorella vulgaris, Chlorococcum littorale, Nannochloropsis oculata, Nannochloropsis sp., Neochloris oleoabundans, Stichococcus bacillaris and Tetraselmis suecica were compared on fatty acid content and productivity, and also on photosynthetic activity under nitrogen (N) starvation. Cultures in N-replete conditions were used as reference. Photosystem II (PSII) maximum efficiency was followed during the experiment, as proxy for the change in photosynthetic activity of the cells. Strains with a high capacity for both lipid accumulation as well as high photosynthetic activity under N starvation exhibited a high lipid productivity over time. Among the tested strains, Nannochloropsis sp. showed highest fatty acid content (45 % w/w) and productivity (238 mg L−1 day−1) as well as PSII maximum efficiency, demonstrating to be the most suitable strain, of those tested, for lipid production. This study highlights that for microalgae, maintaining a high photosynthetic efficiency during stress is the key to maintain high fatty acid productivities overtime and should be considered when selecting strains for microalgal lipid production.


Microalgae Nitrogen starvation Lipid productivity Photosynthetic activity 



The authors would like to thank the Ministry of Economic Affairs, Agriculture and Innovation, the Province of Gelderland, Biosolar Cells, BASF, BioOils, Cellulac, Drie Wilgen Development, DSM, Exxon Mobil, GEA Westfalia Separator, Heliae, Neste Oil, Nijhuis, Paques, Proviron, Roquette, SABIC, Simris Alg, Staatsolie Suriname, Synthetic Genomics, TOTAL and Unilever for financially supporting the AlgaePARC research programme. Thanks to Christa Heryanto for performing the analysis of the fatty acid samples.

Supplementary material

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  1. Berges JA, Falkowski PG (1998) Physiological stress and cell death in marine phytoplankton: induction of proteases in response to nitrogen or light limitation. Limnol Oceanogr 43:129–135CrossRefGoogle Scholar
  2. Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110:689–696PubMedCentralPubMedGoogle Scholar
  3. Bondioli P, Della Bella L, Rivolta G, Zittelli GC, Bassi N, Rodolfi L, Casini D, Prussi M, Chiaramonti D, Tredici MR (2012) Oil production by the marine microalgae Nannochloropsis sp. F&M-M24 and Tetraselmis suecica F&M-M33. Bioresour Technol 114:567–572PubMedCrossRefGoogle Scholar
  4. Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226PubMedCrossRefGoogle Scholar
  5. Cosgrove J, Borowitzka MA (2010) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prásil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17CrossRefGoogle Scholar
  6. Falkowski PG, Owens TG (1980) Light-shade adaptation. Plant Physiol 66:592–595PubMedCentralPubMedCrossRefGoogle Scholar
  7. Geider RJ, Laroche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J Phycol 29:755–766CrossRefGoogle Scholar
  8. Geider R, Graziano L, McKay RM (1998) Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur J Phycol 33:315–332CrossRefGoogle Scholar
  9. Griffiths MJ, Harrison STL (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507CrossRefGoogle Scholar
  10. Griffiths MJ, Hille RP, Harrison STL (2011) Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. J Appl Phycol 24:989–1001CrossRefGoogle Scholar
  11. Hempel F, Bozarth AS, Lindenkamp N, Klingl A, Zauner S, Linne U, Steinbüchel A, Maier UG (2011) Microalgae as bioreactors for bioplastic production. Microb Cell Fact 10:81Google Scholar
  12. Klok AJ, Martens DE, Wijffels RH, Lamers PP (2013) Simultaneous growth and neutral lipid accumulation in microalgae. Bioresour Technol 134:233–243PubMedCrossRefGoogle Scholar
  13. Li Y, Horsman M, Wang B, Wu N, Lan CQ (2008) Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Appl Microbiol Biotechnol 81:629–636PubMedCrossRefGoogle Scholar
  14. Parkhill J, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529CrossRefGoogle Scholar
  15. Pienkos P, Darzins A (2009) The promise and challenges of microalgal-derived biofuels. Biofuels Bioprod Bioref 3:431–440CrossRefGoogle Scholar
  16. Pruvost J, Van Vooren G, Cogne G, Legrand J (2009) Investigation of biomass and lipids production with Neochloris oleoabundans in photobioreactor. Bioresour Technol 100:5988–5995PubMedCrossRefGoogle Scholar
  17. Ramanna L, Guldhe A, Rawat I, Bux F (2014) The optimization of biomass and lipid yields of Chlorella sorokiniana when using wastewater supplemented with different nitrogen sources. Bioresour Technol 168:127–35Google Scholar
  18. Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici M (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112PubMedCrossRefGoogle Scholar
  19. San Pedro A, González-López CV, Acién FG, Molina-Grima E (2013) Marine microalgae selection and culture conditions optimization for biodiesel production. Bioresour Technol 134:353–361Google Scholar
  20. Sauer J, Schreiber U, Schmid R, et al. (2001) Nitrogen starvation-induced chlorosis in synechococcus PCC 7942. Low-level photosynthesis as a mechanism of long-term survival. PLANT Physiol 126:233–243Google Scholar
  21. Schenk PM, Thomas-Hall SR, Stephens E, Marx UC, Mussgnug JH, Posten C, Kruse O, Hankamer B (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenergy Res 1:20–43Google Scholar
  22. Shelly K, Holland D, Beardall J (2011) Assessing nutrient status of microalgae using chlorophyll a fluorescence. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences. Methods and applications. Springer, Dordrecht, pp 223–235Google Scholar
  23. Simionato D, Block MA, La Rocca N, Jouhet J, Maréchal E, Finazzi G, Morosinotto T (2013) The response of Nannochloropsis gaditana to nitrogen starvation includes de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids, and reorganization of the photosynthetic apparatus. Eukaryot Cell 12:665–676PubMedCentralPubMedCrossRefGoogle Scholar
  24. Solovchenko AE, Khozin-Goldberg I, Didi-Cohen S, Cohen Z, Merzlyak MN (2008) Effects of light intensity and nitrogen starvation on growth, total fatty acids and arachidonic acid in the green microalga Parietochloris incisa. J Appl Phycol 20:245–251CrossRefGoogle Scholar
  25. Solovchenko A, Solovchenko O, Khozin-Goldberg I, Didi-Cohen S, Pal D, Cohen Z, Boussiba S (2013) Probing the effects of high-light stress on pigment and lipid metabolism in nitrogen-starving microalgae by measuring chlorophyll fluorescence transients: studies with a Δ5 desaturase mutant of Parietochloris incisa (Chlorophyta, Trebouxiophyceae). Algal Res 2:175–182CrossRefGoogle Scholar
  26. Tredici MR, Biondi N, Ponis E, Rodolfi L, Zitelli GC (2009) Advances in microalgal culture for aquaculture feed and other uses. In: Burnell G. Allan G (ed) New technologies in aquaculture: improving production efficiency, quality and environmental management. Woodhead Publishing, pp 661–676Google Scholar
  27. Van Vooren G, Le Grand F, Legrand J, Cuiné S, Peltier G, Pruvost J (2012) Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Bioresour Technol 124:421–432PubMedCrossRefGoogle Scholar
  28. Vejrazka C, Janssen M, Streefland M, Wijffels RH (2011) Photosynthetic efficiency of Chlamydomonas reinhardtii in flashing light. Biotechnol Bioeng 108:2905–2913PubMedCrossRefGoogle Scholar
  29. White S, Anandraj A, Bux F (2011) PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresour Technol 102:1675–1682Google Scholar
  30. Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799PubMedCrossRefGoogle Scholar
  31. Young EB, Beardall J (2003) Photosynthetic function in Dunaliella tertiolecta (Chlorophyta) during a nitrogen starvation and recovery cycle. J Phycol 905:897–905CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Giulia Benvenuti
    • 1
  • Rouke Bosma
    • 1
  • María Cuaresma
    • 1
  • Marcel Janssen
    • 1
  • Maria J. Barbosa
    • 2
  • René H. Wijffels
    • 1
    • 3
  1. 1.Bioprocess Engineering, AlgaePARCWageningen UniversityBennekomThe Netherlands
  2. 2.Food and Biobased Research, AlgaePARCWageningen University and Research CenterWageningenThe Netherlands
  3. 3.Nordland UniversityBodøNorway

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