Effect of linoleic acid and methyl jasmonate on astaxanthin content of Scenedesmus acutus and Chlorella sorokiniana under heterotrophic cultivation and salt shock conditions

  • Zahra Khalili
  • Hasan JaliliEmail author
  • Mostafa Noroozi
  • Abdeltif Amrane


Aquatic organisms, especially microalgae, are sources of highly bioactive metabolites which could be used in pharmaceutical, biofuels, food, agricultural, and cosmetics industries. In this research, the effect of linoleic acid (LA), as allelochemical and the precursor of two phytohormones, on astaxanthin production in Scenedesmus acutus and Chlorella sorokiniana was investigated under heterotrophic and salt stress conditions. In the absence of salt addition, addition of 32 μM LA after 96 h post inoculation during C. sorokiniana cultivation enhanced cell astaxanthin concentration 1.6 times compared to the control (no addition of LA), while the addition of 160 μM LA during the logarithmic phase of S. acutus enhanced astaxanthin production 10 times compared to the control. In C. sorokiniana under salt stress conditions, the incremental effect of LA on astaxanthin production is expanded, while salt addition did not have significant impact on astaxanthin production during S. acutus culture. In the presence of 20% salt, methyl jasmonate (MJ) treatment produced approximately threefold astaxanthin compared to LA in C. sorokiniana, while the astaxanthin formation for LA and MJ treatment in the presence of 20% salt were roughly equal during S. acutus culture. It can be therefore concluded that LA, as allelochemical and precursor of jasmonic and traumatic acid in oxylipin pathway, has an important role in the astaxanthin production in microalgae. Moreover, for the first time, the potential of LA as an enhancer of algal astaxanthin production was shown.


Astaxanthin content Linoleic acid Salt shock Heterotrophic growth, Chlorophyta 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Affenzeller MJ, Darehshouri A, Andosch A, Lütz C, Lütz-Meindl U (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Bot 60:939–954CrossRefGoogle Scholar
  2. Ahmed F, Fanning K, Netzel M, Schenk PM (2015) Induced carotenoid accumulation in Dunaliella salina and Tetraselmis suecica by plant hormones and UV-C radiation. Appl Microbiol Biotechnol 99:9407–9416CrossRefGoogle Scholar
  3. Assunção MFG, Amaral R, Martins CB, Ferreira JD, Ressurreição S, Santos SD, Varejão JMTB, Santos LMA (2017) Screening microalgae as potential sources of antioxidants. J Appl Phycol 29:865–877CrossRefGoogle Scholar
  4. Barghbani R, Rezaei K, Javanshir A (2012) Investigating the effects of several parameters on the growth of Chlorella vulgaris using Taguchi’s experimental approach. Int J Biotechnol Wellness Ind 1:128–133Google Scholar
  5. Benavente-Valdés JR, Aguilar C, Contreras-Esquivel JC, Méndez-Zavala A, Montañez J (2016) Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnol Rep 10:117–125CrossRefGoogle Scholar
  6. Chen G, Wang B, Han D, Sommerfeld M, Lu Y, Chen F, Hu Q (2015) Molecular mechanisms of the coordination between astaxanthin and fatty acid biosynthesis in Haematococcus pluvialis (Chlorophyceae). Plant J 81:95–107CrossRefGoogle Scholar
  7. Cheng J-S, Niu Y-H, Lu S-H, Yuan Y-J (2012) Metabolome analysis reveals ethanolamine as potential marker for improving lipid accumulation of model photosynthetic organisms. J Chem Technol Biotechno 87:1409–1418CrossRefGoogle Scholar
  8. Christov C, Pouneva I, Bozhkova M, Toncheva T, Fournadzieva S, Zafirova T (2001) Influence of temperature and methyl jasmonate on Scenedesmus incrassulatus. Biol Plant 44:367–371CrossRefGoogle Scholar
  9. Cuellar-Bermudez SP, Aguilar-Hernandez I, Cardenas-Chavez DL, Ornelas-Soto N, Romero-Ogawa MA, Parra-Saldivar R (2015) Extraction and purification of high-value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microb Biotechnol 8:190–209CrossRefGoogle Scholar
  10. Czerpak R, Bajguz A, Gromek M, Kozłowska G, Nowak I (2002) Activity of salicylic acid on the growth and biochemism of Chlorella vulgaris Beijerinck. Acta Physiol Plant 24:45–52CrossRefGoogle Scholar
  11. Czerpak R, Piotrowska A, Szulecka K (2006) Jasmonic acid affects changes in the growth and some components content in alga Chlorella vulgaris. Acta Physiol Plant 28:195–203CrossRefGoogle Scholar
  12. Dao G-H, Wu G-X, Wang X-X, Zhuang L-L, Zhang T-Y, Hu H-Y (2018) Enhanced growth and fatty acid accumulation of microalgae Scenedesmus sp. LX1 by two types of auxin. Bioresour Technol 247:561–567CrossRefGoogle Scholar
  13. Darvish M, Jalili H, Ranaei-Siadat S-O, Sedighi M (2018) Potential cytotoxic effects of peptide fractions from Dunaliella salina protein hydrolyzed by gastric proteases. J Aquat Food Prod Technol 27:165–175CrossRefGoogle Scholar
  14. de la Jara A, Ruano-Rodriguez C, Polifrone M, Assunçao P, Brito-Casillas Y, Wägner AM, Serra-Majem L (2018) Impact of dietary Arthrospira (Spirulina) biomass consumption on human health: main health targets and systematic review. J Appl Phycol 30:2403–2423CrossRefGoogle Scholar
  15. de los Reyes C, Ávila-Román J, Ortega MJ, de la Jara A, García-Mauriño S, Motilva V, Zubía E (2014) Oxylipins from the microalgae Chlamydomonas debaryana and Nannochloropsis gaditana and their activity as TNF-α inhibitors. Phytochemistry 102:152–161CrossRefGoogle Scholar
  16. Del Campo J, Rodriguez H, Moreno J, Vargas M, Rivas J, Guerrero M (2004) Accumulation of astaxanthin and lutein in Chlorella zofingiensis (Chlorophyta). Appl Microbiol Biotechnol 64:848–854CrossRefGoogle Scholar
  17. Engelberth J (2014) Jasmonates and other fatty acid-derived signaling pathways in the plant defense response. In: Zeiger T, Murphy M (eds) Plant physiology and development, 6th edn. Sinauer, New YorkGoogle Scholar
  18. Fedina I, Benderliev K (2000) Response of Scenedesmus incrassatulus to salt stress as affected by methyl jasmonate. Biol Plant 43:625–627CrossRefGoogle Scholar
  19. Gao Z, Meng C, Zhang X, Xu D, Zhao Y, Wang Y, Lv H, Liming Y, Chen L, Ye N (2012) Differential expression of carotenogenic genes, associated changes on astaxanthin production and photosynthesis features induced by JA in H. pluvialis. PloS One 7:e42243CrossRefGoogle Scholar
  20. Gao Z, Meng C, Gao H, Zhang X, Xu D, Su Y, Wang Y, Zhao Y, Ye N (2013a) Analysis of mRNA expression profiles of carotenogenesis and astaxanthin production of Haematococcus pluvialis under exogenous 2,4-epibrassinolide (EBR). Biol Res 46:201–206CrossRefGoogle Scholar
  21. Gao Z, Meng C, Gao H, Li Y, Zhang X, Xu D, Zhou S, Liu B, Su Y, Ye N (2013b) Carotenoid genes transcriptional regulation for astaxanthin accumulation in fresh water unicellular alga Haematococcus pluvialis by gibberellin A3 (GA3). Indian J Biochem Biophys 50:548–553Google Scholar
  22. Hanagata N, Dubinsky Z (1999) Secondary carotenoid accumulation in Scenedesmus komarekii (Chlorophyceae, Chlorophyta). J Phycol 35:960–966CrossRefGoogle Scholar
  23. Henríquez V, Escobar C, Galarza J, Gimpel J (2016) Carotenoids in microalgae. In: Stange C (ed) Carotenoids in nature: biosynthesis, regulation and function. Springer, Cham, pp 219–237CrossRefGoogle Scholar
  24. Imamoglu E, Dalay MC, Sukan FV (2009) Influences of different stress media and high light intensities on accumulation of astaxanthin in the green alga Haematococcus pluvialis. New Biotechnol 26:199–204CrossRefGoogle Scholar
  25. Ip P-F, Chen F (2005) Employment of reactive oxygen species to enhance astaxanthin formation in Chlorella zofingiensis in heterotrophic culture. Process Biochem 40:3491–3496CrossRefGoogle Scholar
  26. Kozlova TA, Hardy BP, Krishna P, Levin DB (2017) Effect of phytohormones on growth and accumulation of pigments and fatty acids in the microalgae Scenedesmus quadricauda. Algal Res 27:325–334CrossRefGoogle Scholar
  27. Lemoine Y, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177CrossRefGoogle Scholar
  28. Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049CrossRefGoogle Scholar
  29. Lin B, Ahmed F, Du H, Li Z, Yan Y, Huang Y, Cui M, Yin Y, Li B, Wang M, Meng C, Gao Z (2018) Plant growth regulators promote lipid and carotenoid accumulation in Chlorella vulgaris. J Appl Phycol 30:1549–1561CrossRefGoogle Scholar
  30. Liu J, Qiu W, Xia D (2018) Brassinosteroid improves lipid productivity and stress tolerance of Chlorella cells induced by high temperature. J Appl Phycol 30:253–260CrossRefGoogle Scholar
  31. Lu Y, Jiang P, Liu S, Gan Q, Cui H, Qin S (2010) Methyl jasmonate- or gibberellins A3-induced astaxanthin accumulation is associated with up-regulation of transcription of beta-carotene ketolase genes (bkts) in microalga Haematococcus pluvialis. Bioresour Technol 101:6468–6474CrossRefGoogle Scholar
  32. Minhas AK, Hodgson P, Barrow CJ, Adholeya A (2016) A review on the assessment of stress conditions for simultaneous production of microalgal lipids and carotenoids. Front Microb 7:1–19CrossRefGoogle Scholar
  33. Ni L, Jie X, Wang P, Li S, Wang G, Li Y, Li Y, Acharya K (2015) Effect of linoleic acid sustained-release microspheres on Microcystis aeruginosa antioxidant enzymes activity and microcystins production and release. Chemosphere 121:110–116CrossRefGoogle Scholar
  34. Pietryczuk A, Czerpak R (2011) Effect of traumatic acid on antioxidant activity in Chlorella vulgaris (Chlorophyceae). Plant Growth Regul 65:279–286CrossRefGoogle Scholar
  35. Pietryczuk A, Piotrowska A, Czerpak R (2008) The influence of traumatic acid on the growth and metabolite content of the green alga Chlorella vulgaris Beijerinck. Oceanol Hydrobiol Stud 37:3–15CrossRefGoogle Scholar
  36. Pietryczuk A, Biziewska I, Imierska M, Czerpak R (2014) Influence of traumatic acid on growth and metabolism of Chlorella vulgaris under conditions of salt stress. Plant Growth Regul 73:103–110CrossRefGoogle Scholar
  37. Qian H, Xu X, Chen W, Jiang H, Jin Y, Liu W, Fu Z (2009) Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 75:368–375CrossRefGoogle Scholar
  38. Qian H, Xu J, Lu T, Zhang Q, Qu Q, Yang Z, Pan X (2018) Responses of unicellular alga Chlorella pyrenoidosa to allelochemical linoleic acid. Sci Total Environ 625:1415–1422CrossRefGoogle Scholar
  39. Raman V, Ravi S (2011) Effect of salicylic acid and methyl jasmonate on antioxidant systems of Haematococcus pluvialis. Acta Physiol Plant 33:1043–1049CrossRefGoogle Scholar
  40. Rumiani LA, Jalili H, Amrane A (2018) Enhanced docosahexaenoic acid production by Crypthecodinium cohnii under combined stress in two-stage cultivation with date syrup based medium. Algal Res 34:75–81CrossRefGoogle Scholar
  41. Salama E-S, Kabra AN, Ji M-K, Kim JR, Min B, Jeon B-H (2014) Enhancement of microalgae growth and fatty acid content under the influence of phytohormones. Bioresour Technol 172:97–103CrossRefGoogle Scholar
  42. Sarada R, Vidhyavathi R, Usha D, Ravishankar GA (2006) An efficient method for extraction of astaxanthin from green alga Haematococcus pluvialis. J Agric Food Chem 54:7585–7588CrossRefGoogle Scholar
  43. Sedighi M, Jalili H, Ranaei-Siadat S-O, Amrane A (2016) Potential health effects of enzymatic protein hydrolysates from Chlorella vulgaris. Appl Food Biotechnol 3:160–169Google Scholar
  44. Solovchenko A (2013) Physiology and adaptive significance of secondary carotenogenesis in green microalgae. Russ J Plant Physiol 60:1–13CrossRefGoogle Scholar
  45. Taiz L, Zeiger E, Møller IMIM, Murphy AS (2014) Plant physiology and development. Sixth edn., p 761Google Scholar
  46. Tarakhovskaya ER, Maslov YI, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physiol 54:163–170CrossRefGoogle Scholar
  47. Wong PK (2000) Effects of 2,4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll-a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere 41:177–182CrossRefGoogle Scholar
  48. Wu J-T, Chiang Y-R, Huang W-Y, Jane W-N (2006) Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria. Aquat Toxicol 80:338–345CrossRefGoogle Scholar
  49. Yang C, Zhou J, Liu S, Fan P, Wang W, Xia C (2013) Allelochemical induces growth and photosynthesis inhibition, oxidative damage in marine diatom Phaeodactylum tricornutum. J Exp Mar Biol Ecol 444:16–23CrossRefGoogle Scholar
  50. Yu X, Chen L, Zhang W (2015) Chemicals to enhance microalgal growth and accumulation of high-value bioproducts. Front Microbiol 6:1–10Google Scholar
  51. Yuan J-P, Chen F, Liu X, Li X-Z (2002) Carotenoid composition in the green microalga Chlorococcum. Food Chem 76:319–325CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Life Science Engineering, Faculty of New Sciences and TechnologiesUniversity of TehranTehranIran
  2. 2.Faculty of Biological SciencesUniversity of AlzahraTehranIran
  3. 3.Ecole Nationale Supérieure de Chimie de Rennes, CNRS, ISCR – UMR6226Univ RennesRennesFrance

Personalised recommendations