Skip to main content
Log in

A strategy for boosting astaxanthin accumulation in green microalga Haematococcus pluvialis by using combined diethyl aminoethyl hexanoate and high light

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

A Correction to this article was published on 13 May 2022

This article has been updated

Abstract

Haematococcus pluvialis is one of the best natural sources of the high-value antioxidant astaxanthin. The use of biotic or abiotic elicitors is an effective strategy to improve astaxanthin production. In this study, a strategy combining diethyl aminoethyl hexanoate (DA-6) and high light was used to promote the accumulation of astaxanthin in H. pluvialis LUGU. The effect of DA-6 on the astaxanthin content, reactive oxygen species (ROS), and transcriptional expression of six astaxanthin biosynthetic genes in H. pluvialis LUGU was investigated. The results showed that treatment with 0.1 mM DA-6 increased the astaxanthin content to 30.95 mg g−1, which was 2.01-fold higher than that of the control (15.43 mg g−1). Moreover, adding exogenous DA-6 significantly accelerated the transcription of chy, pds, and ptox2, which are responsible for substrate conversion and electron transport during the process of astaxanthin formation under conditions of high light. The level of reactive oxygen species (ROS) and the upregulation of astaxanthin biosynthesis-related genes increased astaxanthin accumulation under DA-6 high light conditions. This work is beneficial in developing an efficient strategy for the hyperproduction of astaxanthin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Change history

References

  • Aluru MR, Rodermel SR (2004) Control of chloroplast redox by the immutans terminal oxidase. Physiol Plant 120:4–11

    Article  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Borowitzka MA, Huisman JM, Osborn A (1991) Culture of the astaxanthin-producing green alga Haematococcus pluvialis. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304

    Article  CAS  Google Scholar 

  • Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117

    Article  CAS  Google Scholar 

  • Campos MD, Campos C, Cardoso HG, Simon PW, Oliveira M, Nogales A, Arnholdt-Schmitt B (2016) Isolation and characterization of plastid terminal oxidase gene from carrot and its relation to carotenoid accumulation. Plant Gene 5:13–21

    Article  CAS  Google Scholar 

  • Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G, Kuntz M (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57–68

    Article  CAS  Google Scholar 

  • Ding W, Zhao P, Peng J, Zhao Y, Xu JW, Li T, Yu X (2018) Melatonin enhances astaxanthin accumulation in the green microalga Haematococcus pluvialis by mechanisms possibly related to abiotic stress tolerance. Algal Res 33:256–265

    Article  Google Scholar 

  • Domınguez-Bocanegra AR, Legarreta IG, Jeronimo FM, Campocosio AT (2004) Influence of environmental and nutritional factors in the production of astaxanthin from Haematococcus pluvialis. Bioresour Technol 92:209–214

    Article  Google Scholar 

  • Droop MR (1954) Conditions governing haematochrome formation and loss in the alga Haematococcus pluvialis Flotow. Arch Mikrobiol 20:391–397

    Article  CAS  Google Scholar 

  • Gao Z, Meng C, Zhang X, Xu D, Miao X, Wang Y, Yang L, Lv H, Chen L, Ye N (2012a) Induction of salicylic acid (SA) on transcriptional expression of eight carotenoid genes and astaxanthin accumulation in Haematococcus pluvialis. Enzym Microb Technol 51:225–230

    Article  CAS  Google Scholar 

  • Gao Z, Meng C, Zhang X, Xu D, Zhao Y, Wang Y, Lv H, Yang L, Chen L, Ye N (2012b) Differential expression of carotenogenic genes, associated changes on astaxanthin production and photosynthesis features induced by JA in H. pluvialis. PLoS One 7:e42243

    Article  CAS  Google Scholar 

  • Gao Z, Meng C, Chen YC, Ahmed F, Mangott A, Schenk PM, Li Y (2015) Comparison of astaxanthin accumulation and biosynthesis gene expression of three Haematococcus pluvialis strains upon salinity stress. J Appl Phycol 27:1853–1860

    Article  CAS  Google Scholar 

  • Han D, Li Y, Hu Q (2013) Astaxanthin in microalgae: pathways, functions and biotechnological implications. Algae 28:131–147

    Article  CAS  Google Scholar 

  • Harker M, Tsavalos AJ, Young AJ (1996) Factors responsible for astaxanthin formation in the chlorophyte Haematococcus pluvialis. Bioresour Technol 55:207–214

    Article  CAS  Google Scholar 

  • He S, Wu Q, He Z (2015) Growth-promoting hormone DA-6 assists phytoextraction and detoxification of Cd by ryegrass. Int J Phytoremediation 17:597–603

    Article  CAS  Google Scholar 

  • Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea FM (2006) Astaxanthin: a review of its chemistry and applications. Crit Rev Food Sci 46:185–196

    Article  CAS  Google Scholar 

  • Hong ME, Choi YY, Sim SJ (2016) Effect of red cyst cell inoculation and iron (II) supplementation on autotrophic astaxanthin production by Haematococcus pluvialis under outdoor summer conditions. J Biotechnol 218:25–33

    Article  CAS  Google Scholar 

  • Hunt RW, Chinnasamy S, Bhatnagar A, Das KC (2010) Effect of biochemical stimulants on biomass productivity and metabolite content of the microalga, Chlorella sorokiniana. Appl Biochem Biotechnol 162:2400–2414

    Article  CAS  Google Scholar 

  • Hunt RW, Chinnasamy S, Das KC (2011) The effect of naphthalene-acetic acid on biomass productivity and chlorophyll content of green algae, coccolithophore, diatom, and cyanobacterium cultures. Appl Biochem Biotechnol 164:1350–1365

    Article  CAS  Google Scholar 

  • Ip PF, Wong KH, Chen F (2004) Enhanced production of astaxanthin by the green microalga Chlorella zofingiensis in mixotrophic culture. Process Biochem 39:1761–1766

    Article  CAS  Google Scholar 

  • Jiang Y, Jiang Y, He S, Zhang H, Pan C (2012) Dissipation of diethyl aminoethyl hexanoate (DA-6) residues in pakchoi, cotton crops and soil. Bull Environ Contam Toxicol 88:533–537

    Article  CAS  Google Scholar 

  • Jiang L, Pei H, Hu W, Han F, Zhang L, Hou Q (2015) Effect of diethyl aminoethyl hexanoate on the accumulation of high-value biocompounds produced by two novel isolated microalgae. Bioresour Technol 197:178–184

    Article  CAS  Google Scholar 

  • Kobayashi M, Kakizono T, Nagai S (1991) Astaxanthin production by a green alga, Haematococcus pluvialis accompanied with morphological changes in acetate media. J Biosci Bioeng 71:335–339

    CAS  Google Scholar 

  • Kobayashi M, Kakizono T, Nagai S (1993) Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Appl Environ Microbiol 59:867–873

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Sommerfeld M, Chen F, Hu Q (2008) Consumption of oxygen by astaxanthin biosynthesis: a protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae). J Plant Physiol 165:1783–1797

    Article  CAS  Google Scholar 

  • Li Y, Sommerfeld M, Chen F, Hu Q (2010) Effect of photon flux densities on regulation of carotenogenesis and cell viability of Haematococcus pluvialis (Chlorophyceae). J Appl Phycol 22:253–263

    Article  CAS  Google Scholar 

  • Liang CX, Li YB, Xu JW, Wang JL, Miao XL, Tang YJ, Gu TY, Zhong JJ (2010) Enhanced biosynthetic gene expressions and production of ganoderic acids in static liquid culture of Ganoderma lucidum under phenobarbital induction. Appl Microbiol Biotechnol 86:1367–1374

    Article  CAS  Google Scholar 

  • 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 30:1549–1561

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • 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 β-carotene ketolase genes (bkts) in microalga Haematococcus pluvialis. Bioresour Technol 101:6468–6474

    Article  CAS  Google Scholar 

  • Orosa M, Torres E, Fidalgo P, Abalde J (2000) Production and analysis of secondary carotenoids in green algae. J Appl Phycol 12:553–556

    Article  CAS  Google Scholar 

  • Parjikolaei BR, El-Houri RB, Fretté XC, Christensen KV (2015) Influence of green solvent extraction on carotenoid yield from shrimp (Pandalus borealis) processing waste. J Food Eng 155:22–28

    Article  Google Scholar 

  • Salama ES, Kabra AN, Ji MK, Kim JR, Min B, Jeon BH (2014) Enhancement of microalgae growth and fatty acid content under the influence of phytohormones. Bioresour Technol 172:97–103

    Article  CAS  Google Scholar 

  • Sarada R, Tripathi U, Ravishankar GA (2002) Influence of stress on astaxanthin production in Haematococcus pluvialis grown under different culture conditions. Process Biochem 37:623–627

    Article  CAS  Google Scholar 

  • Shang M, Ding W, Zhao Y, Xu JW, Zhao P, Li T, Yu X (2016) Enhanced astaxanthin production from Haematococcus pluvialis using butylated hydroxyanisole. J Biotechnol 236:199–207

    Article  CAS  Google Scholar 

  • Steinbrenner J, Linden H (2003) Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis: regulation by photosynthetic redox control. Plant Mol Biol 52:343–356

    Article  CAS  Google Scholar 

  • Sun Z, Cunningham FX, Gantt E (1998) Differential expression of two isopentenyl pyrophosphate isomerases and enhanced carotenoid accumulation in a unicellular chlorophyte. Proc Natl Acad Sci U S A 95:11482–11488

    Article  CAS  Google Scholar 

  • Tate JJ, Gutierrez-Wing MT, Rusch KA, Benton MG (2013) The effects of plant growth substances and mixed cultures on growth and metabolite production of green algae Chlorella sp.: a review. J Plant Growth Regul 32:417–428

    Article  CAS  Google Scholar 

  • Torzillo G, Göksan T, Isik O, Gökpinar Ş (2005) Photon irradiance required to support optimal growth and interrelations between irradiance and pigment composition in the green alga Haematococcus pluvialis. Eur J Phycol 40:233–240

    Article  CAS  Google Scholar 

  • Voß U, Bishopp A, Farcot E, Bennett MJ (2014) Modelling hormonal response and development. Trends Plant Sci 19:311–319

    Article  Google Scholar 

  • Wang J, Sommerfeld M, Hu Q (2009) Occurrence and environmental stress responses of two plastid terminal oxidases in Haematococcus pluvialis (Chlorophyceae). Planta 230:191–203

    Article  CAS  Google Scholar 

  • Wen Z, Liu Z, Hou Y, Liu C, Gao F, Zheng Y, Chen F (2015) Ethanol induced astaxanthin accumulation and transcriptional expression of carotenogenic genes in Haematococcus pluvialis. Enzym Microb Technol 78:10–17

    Article  CAS  Google Scholar 

  • Yu X, Niu X, Zhang X, Pei G, Liu J, Chen L, Zhang W (2015) Identification and mechanism analysis of chemical modulators enhancing astaxanthin accumulation in Haematococcus pluvialis. Algal Res 11:284–293

    Article  Google Scholar 

  • Zhang Z, Sun D, Mao X, Liu J, Chen F (2016) The crosstalk between astaxanthin, fatty acids and reactive oxygen species in heterotrophic Chlorella zofingiensis. Algal Res 19:178–183

    Article  Google Scholar 

  • Zhang Z, Sun D, Cheng KW, Chen F (2018) Inhibition of autophagy modulates astaxanthin and total fatty acid biosynthesis in Chlorella zofingiensis under nitrogen starvation. Bioresour Technol 247:610–615

    Article  CAS  Google Scholar 

  • Zhao Y, Shang M, Xu JW, Zhao P, Li T, Yu X (2015) Enhanced astaxanthin production from a novel strain of Haematococcus pluvialis using fulvic acid. Process Biochem 50:2072–2077

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Natural Science Foundation of China (21766012), Key Science and Technology Project of Yunan Province (2018ZG003), the National Natural Science Foundation of China (21666012), and the Health Science and Technology Plan Projects of Yunnan Province, China (2014NS227).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xuya Yu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ding, W., Peng, J., Zhao, Y. et al. A strategy for boosting astaxanthin accumulation in green microalga Haematococcus pluvialis by using combined diethyl aminoethyl hexanoate and high light. J Appl Phycol 31, 171–181 (2019). https://doi.org/10.1007/s10811-018-1561-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1561-8

Keywords

Navigation