Skip to main content
SpringerLink
Log in

Oxidative stress modulates astaxanthin synthesis in Haematococcus pluvialis

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

Abstract

Astaxanthin, a carotenoid with potent antioxidant effects, is produced by the green alga Haematococcus pluvialis in response to stressful environmental conditions. During encystment several cellular shifts occur, such as the initiation of carotenogenesis and accumulation of reactive oxygen species (ROS) intracellularly. While the presence of ROS during encystment has been established, the effect of ROS on carotenogenesis directly is still primarily unknown. In this study, the relationship between astaxanthin accumulation and ROS production were quantified in H. pluvialis. Cellular astaxanthin and ROS concentrations were measured over 14 days in response to the application of environmental variable, redox-sensitive compound, and ROS-scavenger treatments. Application of both environmental and redox-sensitive treatments induced encystment and carotenogenesis. Initial astaxanthin production rates over days 0–4 were highest in the redox-sensitive variable group, with a subsequent rate peak at days 7–9 for environmental test groups. Cellular ROS concentrations similarly peaked over days 0–4 and 7–9 for redox-sensitive and environmental test groups, respectively. All treatment groups later showed significant decreases in ROS concentration by days 11–14. Furthermore, application of ROS-scavenger treatments induced germination and decreased carotenogenesis rates. By quantifying the relationship between astaxanthin and ROS, this work supports the role of ROS as a modulator of carotenogenesis in H. pluvialis and of astaxanthin as a protective mechanism against oxidative stress. Applications of this study can be further applied to design a more optimized technique of commercial astaxanthin production by combining traditional environmental stress conditions with oxidative stress-inducing factors, reducing natural astaxanthin production time requirements by over 10%.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All datasets collected or generated during this study are available by reasonable request.

References

  • Ambati R, Moi P, Ravi S, Aswathanarayana R (2014) Astaxanthin: Sources, extraction, stability, biological activities and its commercial applications - A review. Mar Drugs 12:128–152

    Article  PubMed  PubMed Central  Google Scholar 

  • Aniya Y, Anders M (1992) Activation of rat liver microsomal glutathione S-transferase by hydrogen peroxide: Role for protein-dimer formation. Arch Biochem Biophys 296:611–616

    Article  CAS  PubMed  Google Scholar 

  • Badary O, Taha R, El-Din G, Abdel-Wahab M (2003) Thymoquinone is a potent superoxide anion scavenger. Drug Chem Toxicol 26:87–98

    Article  CAS  PubMed  Google Scholar 

  • Battelli M, Corte E, Stirpe F (1972) Xanthine oxidase type D (dehydrogenase) in the intestine and other organs of the rat. Biochem J 126:747–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhuvaneswari S, Anuradha C (2012) Astaxanthin prevents loss of insulin signaling and improves glucose metabolism in liver of insulin resistant mice. Can J Physiol Pharm 90:1544–1552

    Article  CAS  Google Scholar 

  • Bolann B, Ulvik R (1987) Release of iron from ferritin by xanthine oxidase role of the superoxide radical. Biochem J 243:55–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Capelli B (2007) Natural astaxanthin: King of the carotenoids. Cyanotech, Kailua Kona

  • Choi Y, Hong M, Sim S (2015) Enhanced astaxanthin extraction efficiency from Haematococcus pluvialis via the cyst germination in outdoor culture systems. Process Biochem 50:2275–2280

    Article  CAS  Google Scholar 

  • Christiansen R, Lie O, Torrissen O (1995) Growth and survival of Atlantic salmon, Salmo salar L., fed different dietary levels of astaxanthin. First-feeding fry. Aquacult Nutr 1:189–198

    Article  Google Scholar 

  • Dose J, Matsugo S, Yokokawa H, Koshida Y, Okazaki S, Seidel U, Eggersdorfer M, Rimbach G, Esatbeyoglu T (2016) Free radical scavenging and cellular antioxidant properties of astaxanthin. Int J Mol Sci 17:103

    Article  PubMed Central  Google Scholar 

  • Du F, Hu C, Zhang L, Xu N (2021) Transcriptome analysis reveals the promoting effect of trisodium citrate on astaxanthin accumulation in Haematococcus pluvialis under high light conditions. Aquaculture 543:736978

    Article  CAS  Google Scholar 

  • Fassett R, Coombes J (2011) Astaxanthin: A potential therapeutic agent in cardiovascular disease. Mar Drugs 9:447–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer C, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  CAS  PubMed  Google Scholar 

  • Fraser P, Miura Y, Misawa N (1997) In vitro characterization of astaxanthin biosynthetic enzymes. J Biol Chem 272:6128–6135

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, Meng C, Zhang X, Xu D, Zhao Y, Wang Y, Lv H, Yang L, 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:e42243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goates C, Knutson K (1994) Enhanced permeation of polar compounds through human epidermis. I. Permeability and membrane structural changes in the presence of short chain alcohols. BBA-Biomembranes 1195:169–179

    Article  CAS  PubMed  Google Scholar 

  • Goldstein S, Czapski G (1984) Mannitol as an OH· scavenger in aqueous solutions and in biological systems. Int J Radiat Biol Res 46:725–729

    CAS  Google Scholar 

  • Hadjzadeh M, Mohammadian N, Rahmani Z, Rassouli F (2008) Effect of thymoquinone on ethylene glycol-induced kidney calculi in rats. Urol J 5:149–155

    PubMed  Google Scholar 

  • He P, Duncan J, Barber J (2007) Astaxanthin accumulation in the green alga Haematococcus pluvialis: Effects of cultivation parameters. J Integr Plant Biol 49:447–451

    Article  CAS  Google Scholar 

  • Hu C, Cui D, Sun X, Shi J, Song L, Li Y, Xu N (2019) Transcriptomic analysis unveils survival strategies of autotrophic Haematococcus pluvialis against high light stress. Aquaculture 513:734430

    Article  CAS  Google Scholar 

  • Ip P, Chen F (2005) Employment of reactive oxygen species to enhance astaxanthin formation in Chlorella zofingiensis in heterotrophic culture. Process Biochem 40:3491–3496

    Article  CAS  Google Scholar 

  • Jomova K, Baros S, Valko M (2012) Redox active metal-induced oxidative stress in biological systems. Transit Metal Chem 37:127–134

    Article  CAS  Google Scholar 

  • Kim Y, Matter I, Lee N, Jung M, Lee Y, Choi S, Lee S, Kim J, Oh Y (2020) Enhancement of astaxanthin production by Haematococcus pluvialis using magnesium aminoclay nanoparticles. Bioresour Technol 307:123270

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi M, Kakizono T, Nishio N, Nagai S, Kurimura Y, Tsuji Y (1997) Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Appl Microbiol Biot 48:351–356

    Article  CAS  Google Scholar 

  • Lee D, Lee Y (2011) Astaxanthin protects against MPTP/MPP+-induced mitochondrial dysfunction and ROS production in vivo and in vitro. Food Chem Toxicol 49:271–280

    Article  CAS  PubMed  Google Scholar 

  • Lepetit B, Sturm S, Rogato A, Gruber A, Sachse M, Falciatore A, Kroth P, Lavaud J (2013) High light acclimation in the secondary plastids containing diatom Phaeodactylum tricornutum is triggered by the redox state of the plastoquinone pool. Plant Physiol 161:853–865

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Li J, Zhu D, Niu J, Shen S, Wang G (2011) An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnol Adv 29:568–574

    Article  CAS  PubMed  Google Scholar 

  • Li F, Cai M, Lin M, Huang X, Wang J, Zheng X, Wu S, An Y (2019) Accumulation of astaxanthin was improved by the nonmotile cells of Haematococcus pluvialis. Biomed Res Int 2019:8101762

    PubMed  PubMed Central  Google Scholar 

  • Lin KH, Lin KC, Lu W, Thomas P, Jayakumar T, Sheu J (2015) Astaxanthin, a carotenoid, stimulates immune responses by enhancing IFN-γ and Il-2 secretion in primary cultured lymphocytes in vitro and ex vivo. Int J Mol Sci 17:44

    Article  PubMed Central  Google Scholar 

  • Martin H, Jäger C, Ruck C, Schmidt M, Walsh R, Paust J (1999) Anti- and prooxidant properties of carotenoids. J Prakt Chemie 341:302–308

    Article  CAS  Google Scholar 

  • März U (2018) The Global Market for Carotenoids. BCC Publishing, Wellesley, Massachusetts, pp 1–146

    Google Scholar 

  • McCall B, McPartland C, Moore R, Frank-Kamenetskii BB (2018) Effects of astaxanthin on the proliferation and migration of breast cancer cells in vitro. Antioxidants 7:135

    Article  PubMed Central  Google Scholar 

  • Panis G, Carreon J (2016) Commercial astaxanthin production derived by green alga Haematococcus pluvialis: A microalgae process model and a techno-economic assessment all through production line. Algal Res 18:175–190

    Article  Google Scholar 

  • Park E, Lee C (2001) Astaxanthin production by Haematococcus pluvialis under various light intensities and wavelengths. J Microbiol Biotechnol 11:1024–1030

    CAS  Google Scholar 

  • Park J, Chyun J, Kim Y, Line L, Chew B (2010) Astaxanthin decreased oxidative stress and inflammation and enhanced immune response in humans. Nutr Metab 7:18

    Article  Google Scholar 

  • Pospíšil P (2016) Production of Reactive oxygen species by photosystem II as a response to light and temperature stress. Front Plant Sci 7:1950

    Article  PubMed  PubMed Central  Google Scholar 

  • RStudio Team (2020) RStudio: Integrated development environment for R, 1.3.1073 edn., Rstudio, Boston

  • Schneegurt M (1998) Cyanosite. Bold’s Basal (BB) Medium. World-wide electronic publication, Wichita State University, Wichita. https://www-cyanosite.bio.purdue.edu; searched on 1 November 2019.

  • Schroeder W, Johnson E (1995) Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma. J Biol Chem 270:18374–18379

    Article  CAS  PubMed  Google Scholar 

  • Shah M, Liang Y, Cheng J, Daroch M (2016) Astaxanthin-producing green microalga Haematococcus pluvialis: From single cell to high value commercial products. Front Plant Sci 7:531

    Article  PubMed  PubMed Central  Google Scholar 

  • Shahidi F, Zhong Y (2015) Measurement of antioxidant activity. J Funct Foods 18:757–781

    Article  CAS  Google Scholar 

  • Shen B, Jensen R, Bohnert H (1997) Mannitol protects against oxidation by hydroxyl radicals. Plant Physiol 115:527–532

    Article  CAS  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • Steinbrenner J (2006) Regulation der Astaxanthinbiosynthese in der Grünalge Haematococcus pluvialis. PhD Thesis, University of Konstanz, 109 pp

  • Su Y, Wang J, Shi M, Niu X, Yu X, Gao L, Zhang X, Chen L, Zhang W (2014) Metabolomic and network analysis of astaxanthin-producing Haematococcus pluvialis under various stress conditions. Bioresour Technol 170:522–529

    Article  CAS  PubMed  Google Scholar 

  • Suganya V, Asheeba S (2015) Antioxidant and antimicrobial activity of astaxanthin isolated from three varieties of crabs. Int J Recent Sci Res 6:6753–6758

    Google Scholar 

  • Sztretye M, Dienes B, Gönczi M, Czirják T, Csernoch L, Dux L, Szentesi K-P (2019) Astaxanthin: A potential mitochondrial-targeted antioxidant treatment in diseases and with aging. Oxid Med Cell Longev 2019:3849692

    Article  PubMed  PubMed Central  Google Scholar 

  • Tan S, Cunningham F, Youmans M, Grabowski B, Sun Z, Gantt E (2008) Cytochrome f loss in astaxanthin-accumulating red cells of Haematococcus pluvialis (Chlorophyeae): Comparison of photosynthetic activity, photosynthetic enzymes, and thylakoid membrane polypeptides in red and green cells. J Phycol 31:897–905

    Article  Google Scholar 

  • Vidhyavathi R, Venkatachalam L, Sandesh Kamath B, Sarada R, Ravishankar G (2007) Differential expression of carotenogenic genes and associated changes in pigment profile during regeneration of Haematococcus pluvialis cysts. Appl Microb Biot 75:879–887

    Article  CAS  Google Scholar 

  • Wang B, Zarka A, Trebst A, Boussiba S (2003) Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance. J Phycol 39:1116–1124

    Article  CAS  Google Scholar 

  • Zhang C, Liu J, Zhang L (2017) Cell cycles and proliferation patterns in Haematococcus pluvialis. Chin J Oceanol Limnol 35:1205–1211

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Tryggvi Stefánsson for supplying algal cultures and technical advice, Schonna Manning for algal culture advice, and Jeffrey Walker for statistical analysis assistance.

Funding

This research was supported by the Maine Economic Improvement Fund (6250254) and the University of Southern Maine Department of Biology Graduate Research Fund.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Southern Maine, Portland, ME, 04103, USA

    Rachel Cray

  2. Department of Natural and Applied Sciences, University of Southern Maine, Portland, ME, 04103, USA

    Ira Levine

Authors
  1. Rachel Cray
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ira Levine
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rachel Cray.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cray, R., Levine, I. Oxidative stress modulates astaxanthin synthesis in Haematococcus pluvialis. J Appl Phycol 34, 2327–2338 (2022). https://doi.org/10.1007/s10811-022-02792-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-022-02792-1

Keywords

Search

Navigation