Advertisement

Applied Microbiology and Biotechnology

, Volume 99, Issue 22, pp 9407–9416 | Cite as

Induced carotenoid accumulation in Dunaliella salina and Tetraselmis suecica by plant hormones and UV-C radiation

  • Faruq Ahmed
  • Kent Fanning
  • Michael Netzel
  • Peer M. Schenk
Biotechnological products and process engineering

Abstract

Carotenoids prevent different degenerative diseases and improve human health. Microalgae are commercially exploited for carotenoids, including astaxanthin and β-carotene. Two commercially important microalgae, Dunaliella salina and Tetraselmis suecica, were treated with plant hormones salicylic acid (SA) and methyl jasmonate (MJ), or by UV-C radiation (T. suecica only) and a combination thereof. Significant increases in total carotenoids were found for D. salina and T. suecica after treatment with MJ (10 μmol/L) and SA (70–250 μmol/L), respectively. T. suecica also had significant increases in total carotenoids following UV-C radiation compared to control cultures. Among the carotenoids, lutein was the highest induced carotenoid. A combination of these two treatments also showed a significant increase in total carotenoids and lutein for T. suecica, when compared to controls. Plant hormones and UV-C radiation may be useful tools for increasing carotenoid accumulation in green microalgae although the responses are species- and dose-specific and should be trialed in medium to large scale to explore commercial production.

Keywords

Carotenoids Methyl jasmonate Microalgae Salicylic acid UV-C radiation 

Notes

Acknowledgments

The authors wish to thank the Australian Research Council and Meat & Livestock Australia for financial support and Dr. Kalpesh Sharma for useful advice on UV-C treatments.

Funding

This study was funded by Meat and Livestock Australia (B.NBP.0695), the Australian Research Council (LP0990558), and an Australian Postgraduate Award (to FA).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

253_2015_6792_MOESM1_ESM.pdf (310 kb)
ESM 1 (PDF 310 kb)

References

  1. Abd El-Baky H, El Baz FK, El-Baroty GS (2004) Production of antioxidant by the green alga Dunaliella salina. Int J Agric Biol 6(1):49–57Google Scholar
  2. Ahmed F, Fanning K, Netzel M, Turner W, Li Y, Schenk PM (2014) Profiling of carotenoids and antioxidant capacity of microalgae from subtropical coastal and brackish waters. Food Chem 165:300–306CrossRefPubMedGoogle Scholar
  3. Böhm F, Edge R, Truscott G (2012) Interactions of dietary carotenoids with activated (singlet) oxygen and free radicals: potential effects for human health. Mol Nutr Food Res 56(2):205–216CrossRefPubMedGoogle Scholar
  4. Borowitzka MA (2013) High-value products from microalgae-their development and commercialisation. J Appl Phycol 25(3):1–14CrossRefGoogle Scholar
  5. Borowitzka MA, Borowitzka LJ, Kessly D (1990) Effects of salinity increase on carotenoid accumulation in the green alga Dunaliella salina. J App Phyc 2:111–119Google Scholar
  6. Chini Zitelli G, Rodolfi L, Biondi N, Tredici MR (2006) Productivity and photosynthetic efficiency of outdoor cultures of Tetraselmis suecica in annular columns. Aquaculture 261:932–943CrossRefGoogle Scholar
  7. Cordero BF, Obraztsova I, Couso I, Leon R, Vargas MA, Rodriguez H (2011) Enhancement of lutein production in Chlorella sorokiniana (chlorophyta) by improvement of culture conditions and random mutagenesis. Mar Drugs 9:1607–1624CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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(1):45–52CrossRefGoogle Scholar
  9. 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(3):195–203CrossRefGoogle Scholar
  10. Del Campo JA, Moreno J, Rodriguez H, Vargas MA, Rivas J, Guerrero MG (1999) Carotenoid content of chlorophycean microalgae: factors determining lutein accumulation in Muriellopsis sp. (Chlorophyta). J Biotechnol 76:51–59CrossRefGoogle Scholar
  11. Demmig-Adams B (1990) Carotenoids and photoprotection: a role for the xanthophylls zeaxanthin. Biochim Biophys Acta 1020:1–24CrossRefGoogle Scholar
  12. Döhler G, Drebes G, Lohmann M (1997) Effect of UV-A and UV-B radiation on pigments, free amino acids and adenylate content of Dunaliella tertiolecta. J Photochem Photobiol 40:126–131CrossRefGoogle Scholar
  13. Duong VT, Li Y, Nowak E, Schenk PM (2012) Microalgae isolation and selection for prospective biodiesel production. Energies 5:1835–1849CrossRefGoogle Scholar
  14. Fedina IS, Benderliev KM (2000) Response of Scenedesmus incrassatulus to salt stress as affected by methyl jasmonate. Biol Plant 43(4):625–627CrossRefGoogle Scholar
  15. Fernandez-Sevilla JM, Acien Fernandez FG, Molina Grima E (2010) Biotechnological production of lutein and its applications. Appl Microbiol Biotechnol 86(1):27–40CrossRefPubMedGoogle Scholar
  16. Fitzgerald KC, O'Reilly ÉJ, Fondell E, Falcone GJ, McCullough ML, Park Y, Kolonel LN, Ascheria A (2013) Intakes of vitamin C and carotenoids and risk of amyotrophic lateral sclerosis: pooled results from 5 cohort studies. Ann Neurol 73:236–245CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fu W, Paglia G, Magnusdottir M, Steinarsdottir E, Gudmundsson S, Palsson B (2014) Effects of abiotic stressors on lutein production in the green microalga Dunaliella salina. Micro Cell Fact 13(1):3CrossRefGoogle Scholar
  18. Fung IP (2005) Elicitation of astaxanthin biosynthesis in darkheterotrophic cultures of Chlorella zofingiensis. PhD thesis, The University of Hong Kong, Hong KongGoogle Scholar
  19. Jung S (2004) Effect of chlorophyll reduction in Arabidopsis thaliana by methyl jasmonate or norflurazon on antioxidant systems. Plant Phys Biochem 42:225–231Google Scholar
  20. Gao Z, Meng C, Zhang X, Xu D, Zhao Y, Wang Y (2012a) Differential expression of carotenogenic genes, associated changes on astaxanthin production and photosynthesis features induced by JA in H. pluvialis. PLoS One 7(8):e42243CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gao Z, Meng C, Zhang X, Xu D, Miao X, Wang Y (2012b) Induction of salicylic acid (SA) on transcriptional expression of eight carotenoid genes and astaxanthin biosynthesis in Haematococcus pluvialis. Enzym Microb Technol 51(4):225–230CrossRefGoogle Scholar
  22. Guedes AC, Amaro HM, Malcata FX (2011) Microalgae as sources of carotenoids. Mar Drugs 9(4):625–644CrossRefPubMedPubMedCentralGoogle Scholar
  23. Huang JJ-H, Cheung PC-K (2011) +UVA treatment increases the degree of unsaturation in microalgal fatty acids and total carotenoid content in Nitzschia closterium (Bacillariophyceae) and Isochrysis zhangjiangensis (Chrysophyceae). Food Chem 129(3):783–791CrossRefPubMedGoogle Scholar
  24. Ibañez E, Cifuentes A (2013) Benefits of using algae as natural sources of functional ingredients. J Sci Food Agric 93(4):703–709CrossRefPubMedGoogle Scholar
  25. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193CrossRefPubMedGoogle Scholar
  26. Jin E, Feth B, Melis A (2003) A mutant of the green alga Dunaliella salina constitutively accumulates zeaxanthin under all growth conditions. Biotechnol Bioeng 81:115–124CrossRefPubMedGoogle Scholar
  27. Lim DKY, Garg S, Timmins M, Zhang ESB, Thomas-Hall SR, Schuhmann H, Li Y, Schenk PM (2012) Isolation and evaluation of oil-producing microalgae from subtropical coastal and brackish waters. PLoS ONE 7:e40751CrossRefPubMedPubMedCentralGoogle Scholar
  28. Liu LH, Zabaras D, Bennett LE, Aguas P, Woonton BW (2009) Effects of UV-C, red light and sun light on the carotenoid content and physical qualities of tomatoes during post-harvest storage. Food Chem 115:495–500CrossRefGoogle Scholar
  29. Lu Y, Jiang P, Liu S, Gan Q, Cui H, Qin S (2010) Methyl jasmona te- or gibberellins A3-induced astaxanthin biosynthesis is associated with up-regulation of transcription of beta-carotene ketolase genes (bkts) in microalga Haematococcus pluvialis. Bioresour Technol 101(16):6468–6474CrossRefPubMedGoogle Scholar
  30. Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K (2005) Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem Biophys Res Commun 332(2):392–397CrossRefPubMedGoogle Scholar
  31. Mogedas B, Casal C, Forján E, Vílchez C (2009) β-Carotene production enhancement by UV-A radiation in Dunaliella bardawil cultivated in laboratory reactors. J Biosci Bioeng 108(1):47–51CrossRefPubMedGoogle Scholar
  32. Pérez-López P, González-García S, Ulloa RG, Sineiro J, Feijoo G, Moreira MT (2014) Life cycle assessment of the production of bioactive compounds from Tetraselmis suecica at pilot scale. J Clean Prod 64:323–331CrossRefGoogle Scholar
  33. Raman V, Ravi S (2011) Effect of salicylic acid and methyl jasmonate on antioxidant systems of Haematococcus pluvialis. Acta Physiol Plant 33(3):1043–1049CrossRefGoogle Scholar
  34. Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB (1997) Influence of salicylic acid on H2O2 production, oxidative stress and H2O2 metabolizing enzymes. Plant Phys 115:137–149Google Scholar
  35. Salguero A, Leon R, Mariotti A, de la Morena B, Vega JM, Vilchez C (2005) UV-A mediated induction of carotenoid biosynthesis in Dunaliella bardawil with retention of cell viability. Appl Microbiol Biotechnol 66(5):506–511CrossRefPubMedGoogle Scholar
  36. Schalch W, Cohn W, Barker FM, Köpcke W, Mellerio J, Bird AC, Robson AG, Fitzke FF, van Kuijk FJGM (2007) Xanthophyll biosynthesis in the human retina during supplementation with lutein or zeaxanthin - the LUXEA (Lutein Xanthophyll Eye Accumulation) study. Arch Biochem Biophys 458(2):128–135CrossRefPubMedGoogle Scholar
  37. Sharma K, Li Y, Schenk PM (2014) UV-C-mediated lipid induction and settling, a step change towards economical microalgal biodiesel production. Green Chem 16:3539CrossRefGoogle Scholar
  38. Sies H, Stahl W (2005) New horizons in carotenoid research. In: Packer L, Obermüller-Jevic U, Kraemer K, Sies H (eds) Carotenoids and retinoids: molecular aspects and health issues. AOCS Press, Urbana, pp 315–320Google Scholar
  39. Stahl W, Sies H (2012) Photoprotection by dietary carotenoids: Concept, mechanisms, evidence and future development. Mol Nutr Food Res 56(2):287–95Google Scholar
  40. Wang CY, Chen CT, Wang SY (2009) Changes of flavonoid content and antioxidant capacity in blueberries after illumination with UV-C. Food Chem 117:426–431CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Faruq Ahmed
    • 1
  • Kent Fanning
    • 2
  • Michael Netzel
    • 3
  • Peer M. Schenk
    • 1
  1. 1.Algae Biotechnology Laboratory, School of Agriculture and Food SciencesThe University of QueenslandBrisbaneAustralia
  2. 2.Department of Agriculture, Fisheries and Forestry (DAFF)Coopers PlainsAustralia
  3. 3.Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation (QAAFI)The University of QueenslandBrisbaneAustralia

Personalised recommendations