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Fast-track production of astaxanthin by reduced cultivation time with the “red cell inoculation system” (RCIS) and various chemical cues in Haematococcus lacustris

  • Sang-Ah Lee
  • Nakyeong Lee
  • Hee-Mock Oh
  • Dae Geun Kim
  • Chi-Yong AhnEmail author
Article

Abstract

Slow growth is the major obstacle in the production of astaxanthin in Haematococcus lacustris. Introduction of a “red cell inoculation system (RCIS)” reduced the culture time of H. lacustris by 43% by increasing its growth rate and inducing the earlier synthesis of astaxanthin. Red mature H. lacustris cells rather than green cyst cells were re-inoculated to decrease the growth period from 7 to 4 days by producing more zoospore cells. Starved red cells could take up nutrients quickly, thereby achieving faster growth. To further shorten the astaxanthin induction time, FeSO4, NaCl, and NaHCO3 were added to the cells, and their effects were compared. These chemicals accelerated astaxanthin biosynthesis, decreasing the production period from 7 to 4 days. This study focused on faster astaxanthin production to achieve economic feasibility by RCIS and chemical cues. Fast-track growth and a synthesis induction strategy enabled a more economic and efficient production of astaxanthin in H. lacustris.

Keywords

Haematococcus lacustris Astaxanthin Red cell inoculation system (RCIS) Chemical cues 

Notes

Funding information

This work was supported by the Korea Research Institute of Bioscience and Biotechnology (KRIBB) Research Initiative Program and the Advanced Biomass R&D Center (ABC), a Global Frontier Program funded by the Korean Ministry of Science and the ICT (2010-0029723).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10811_2019_1904_MOESM1_ESM.docx (951 kb)
ESM 1 (DOCX 951 kb)

References

  1. Alessandro C, Massimo P, Giacomo C (2015) Disruption of microalgal cells for lipid extraction through Fenton reaction: modeling of experiments and remarks on its effect on lipids composition. Chem Eng J 263:392–401CrossRefGoogle Scholar
  2. Alizadeh G, Jalilova A, Aliev I, Magerramova KK (2017) Carotenogenesis in Dunaliella cells under stressed conditions. Eur J Biotechnol Biosci 5:41–46Google Scholar
  3. Andrewes G, Starr MP (1976) (3R-3’R)-astaxanthin from the yeast Phaffia rhodozyma. Phytochemistry 15:1009–1011CrossRefGoogle Scholar
  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  5. APHA (2005) Standard methods for the examination of water and wastewater 20rd edition. Water Environment Federation, USAGoogle Scholar
  6. Benavente-Valdes JR, Aguilar C, Contreras-Esquivel JC, Mendez-Zavala A, Montanez J (2016) Strategies to enhance the production of photosynthetic pigments and lipids in chlorophycae species. Biotechnol Rep 10:117–125Google Scholar
  7. Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Biochim Biophys Acta 1758:994–1003Google Scholar
  8. Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117Google Scholar
  9. Boussiba S, Ring W, Yuan J, Zarka A, Chen F (1999) Changes in pigments profile in the green alga Haematococcus pluvialis exposed to environmental stresses. Biotechnol Lett 21:601–604CrossRefGoogle Scholar
  10. Brambilla F, Forchino A, Antonini M, Rimoldi S, Terova G, Saroglia M (2009) Effect of dietary astaxanthin sources supplementation on muscle pigmentation and lipid peroxidation in rainbow trout (Oncorhynchus mykiss). Ital J Anim Sci 8:845–847CrossRefGoogle Scholar
  11. Burg SP, Burg EA (1965) Ethylene action and the ripening of fruits: ethylene influences the growth and development of plants and is the hormone which initiates fruit ripening. Science 148:1190–1196CrossRefGoogle Scholar
  12. Capelli B, Bagchi D, Cysewski GR (2013) Synthetic astaxanthin is significantly inferior to algal-based astaxanthin as an antioxidant and may not be suitable as a human nutraceutical supplement. Nutrafoods 12:145–152CrossRefGoogle Scholar
  13. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306CrossRefGoogle Scholar
  14. Choi SK, Kim JH, Park YS, Kim YJ, Chang HI (2007) An efficient method for the extraction of astaxanthin from the red yeast Xanthophyllomyces dendrorhous. J Microbiol Biotechnol 17:847–852Google Scholar
  15. Chokshi K, Pancha I, Ghosh A, Mishra S (2017) Nitrogen starvation-induced cellular crosstalk of ROS-scavenging antioxidants and phytohormone enhanced the biofuel potential of green microalga Acutodesmus dimorphus. Biotechnol Biofuels 60:1–12Google Scholar
  16. Cordero B, Otero A, Parino M, Arredondo BO, Fabregas J (1996) Astaxanthin production from the green alga Haematococcus pluvialis with different stress conditions. Biotechnol Lett 18:213–218CrossRefGoogle Scholar
  17. Dong S, Huang Y, Zhang R, Wang S, Liu Y (2014) Four different methods comparison for extraction of astaxanthin from green alga Haematococcus pluvialis. Sci World J 1:1–7Google Scholar
  18. Fabregas J, Dominguez A, Regueiro M, Maseda A, Otero A (2000) Optimization of culture medium for the continuous cultivation of the microalga Haematococcus pluvialis. Appl Microbiol Biotechnol 53:530–535CrossRefGoogle Scholar
  19. Fabregas J, Dominguez A, Maseda A, Otero A (2003) Interactions between irradiance and nutrient availability during astaxanthin accumulation and degradation in Haematococcus pluvialis. Appl Microbiol Biotechnol 61:545–551CrossRefGoogle Scholar
  20. Gao Z, Meng C, Zhang X, Xu D, Zhao Y, Wang Y, Lv H, Yang L, Chen L, Ye N (2012) Differential expression of carotenogenetic genes, associated changes on astaxanthin production and photosynthesis features induced by JA in H. pluvialis. PLoS One 7:e42243CrossRefGoogle Scholar
  21. Gao Z, Meng C, Gao H, Zhang X, Su Y, Ye N (2013) The induction of ferrous sulfate or sodium acetate on mRNA expression of carotenoid gene in Haematococcus pluvialis. Res J Biotechnol 8:43–50Google Scholar
  22. Gao Z, Meng C, Chen YC, Ahmed F, Schenk PM, Li Y (2015) Comparison of astaxanthin accumulation and biosynthesis gene expression of three Haematococcus pluvialis strains upon salinity stress. J Appl Phycol 27:1853–1860CrossRefGoogle Scholar
  23. Gong X, Chen F (1998) Influence of medium components on astaxanthin content and production of Haematococcus pluvialis. Process Biochem 33:385–391CrossRefGoogle Scholar
  24. Grung M, D’Souza FML, Borowitzka M, Liaaen-Jensen S (1992) Algal carotenoids 51. Secondary carotenoids 2. Haematococcus pluvialis aplanospores as a source of (3S, 3′S)-astaxanthin esters. J Appl Phycol 4:165–171CrossRefGoogle Scholar
  25. Guerin M, Huntley ME, Olaizola M (2003) Haematococcus pluvialis: applications for human health and nutrition. Trends Biotechnol 21:210–216CrossRefGoogle Scholar
  26. Harker M, Tsavalos AJ, Young AJ (1996) Factors responsible for astaxanthin formation in the chlorophyte Haematococcus pluvialis. Bioresour Technol 55:207–214CrossRefGoogle Scholar
  27. Hong ME, Choi YY, Sim SJ (2016) Effect of red cyst inoculation and iron (II) supplementation on autotrophic astaxanthin production by Haematococcus pluvialis under outdoor summer conditions. J Biotechnol 218:25–33CrossRefGoogle Scholar
  28. Iigusa H, Yoshida Y, Hasunuma K (2005) Oxygen and hydrogen peroxide enhance light-induced carotenoid synthesis in Neurospora crassa. FEBS Lett 579:4012–4016CrossRefGoogle Scholar
  29. Jansson M (1993) Uptake, exchange and excretion of orthophosphate in phosphate-starved Scenedesmus quadricauda and Pseudomonas K7. Limnol Oceanogr 38:1162–1178CrossRefGoogle Scholar
  30. Jia D, Fan L, Shen J, Liu C, Yuan Y, Qin S, Cui C (2014) Biological synthesis of astaxanthin in apple callus by genetic transformation of bkt and crtR-B from Haematococcus pluvialis. Acta Hortic 1048: International:143–149CrossRefGoogle Scholar
  31. Jin ES, Lee CG, Polle JEW (2006) Secondary carotenoid accumulation in Haematococcus (Chlorophyceae): biosynthesis, regulation, and biotechnology. J Microbiol Biotechnol 16:821–831Google Scholar
  32. Kang CD, An JY, Park TH, Sim SJ (2006) Astaxanthin biosynthesis from simultaneous N and P uptake by the green alga Haematococcus pluvialis in primary-treated wastewater. Biochem Eng J 31:234–238CrossRefGoogle Scholar
  33. Lee CS, Choi YE, Yun YS (2016) A strategy for promoting astaxanthin accumulation in Haematococcus pluvialis by 1-aminocyclopropane-1-carboxylic acid application. J Biotechnol 236:120–127CrossRefGoogle Scholar
  34. Mahfuzur M, Shah R, Liang Y, Cheng JJ, Daroch M (2016) Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Front Plant Sci 7:531Google Scholar
  35. Naguib YMA (2000) Antioxidant activities of astaxanthin and related carotenoids. J Agric Food Chem 48:1150–1154CrossRefGoogle Scholar
  36. Nakada T, Ota S (2016) What is the correct name for the type of Haematococcus Flot. (Volvocales, Chlorophyceae)? Taxon 65:343–348CrossRefGoogle Scholar
  37. Ota S, Morita A, Ohnuki S, Hirata A, Sekida S, Okuda K, Ohya Y, Kawano S (2018) Carotenoid dynamics and lipid droplet containing astaxanthin in response to light in the green alga Haematococcus pluvialis. Sci Rep 8:5617CrossRefGoogle Scholar
  38. Puckette MC, Weng H, Mahalingam R (2007) Physiological and biochemical responses to acute ozone-induced oxidative stress in Medicago truncatula. Plant Physiol Biochem 45:70–79CrossRefGoogle Scholar
  39. Scaife MA, Ma CA, Armenta RE (2012) Efficient extraction of canthaxanthin from Escherichia coli by a 2-step process with organic solvents. Bioresour Technol 111:276–281CrossRefGoogle Scholar
  40. Shimidzu N, Goto M, Miki W (1996) Carotenoids as singlet oxygen quenchers in marine organisms. Fish Sci 62:134–137CrossRefGoogle Scholar
  41. Sim SJ, Hong ME (2015) Method for increasing a productivity of astaxanthin in Haematococcus pluvialis by marine cyst inoculated and iron ions mediated Haber-Weiss reaction at high temperature. Korea Patent 10-2015-0048444, April 06, 2015Google Scholar
  42. Soto P, Gaete H, Hidalgo ME (2011) Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and growth rate in the freshwater green algae Pseudokirchneriella subcapitata exposed to copper and zinc. Lat Am Aquat Res 39:280–285CrossRefGoogle Scholar
  43. Sun XM, Ren LJ, Zhao QY, Ji XJ, Huang H (2018) Microalgae for the production of lipid and carotenoids: a review with focus on stress regulation and adaptation. Biotechnol Biofuels 11:272CrossRefGoogle Scholar
  44. Vidhyavathi R, Venkatachalam L, Sarada R, Ravishankar GA (2008) Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions. J Exp Bot 59:1409–1418CrossRefGoogle Scholar
  45. Vo T, Lee CS, Han SI, Kim JY, Kim S, Choi YE (2016) Effect of the ethylene precursor, 1-aminocyclopropane-1-carboxylic acid on different growth stages of Haematococcus pluvialis. Bioresour Technol 220:85–93CrossRefGoogle Scholar
  46. Wang WB, Kim YH, Lee HS, Kim KY, Deng XP, Kwak SS (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Biochem 47:570–577CrossRefGoogle Scholar
  47. Wang J, Han D, Sommerfeld MR, Lu C, Hu Q (2013) Effect of initial biomass density on growth and astaxanthin production of Haematococcus pluvialis in an outdoor photobioreactor. J Appl Phycol 25:253–260CrossRefGoogle Scholar
  48. Xuan RR, Niu TT, Chen HM (2016) Astaxanthin blocks preeclampsia progression by suppressing oxidative stress and inflammation. Mol Med Rep 14:2697–2704CrossRefGoogle Scholar
  49. Yang Y, Kim B, Lee JY (2013) Astaxanthin structure, metabolism, and health benefits. J Hum Nutr Food Sci 1:1003Google Scholar
  50. Zhang C, Liu J, Zhang L (2017) Cell cycles and proliferation patterns in Haematococcus pluvialis. Chin J Oceanol Limnol 35:1205–1211CrossRefGoogle Scholar
  51. Zhekisheva M, Boussiba S, Goldberg IK, Zarka A, Cohen Z (2002) Accumulation of oleic acid in Haematococcus pluvialis (Chlorophyceae) under nitrogen starvation or high light is correlated with that of astaxanthin esters. J Phycol 38:325–331CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Cell Factory Research CenterKorea Research Institute of Bioscience and Biotechnology (KRIBB)DaejeonRepublic of Korea
  2. 2.Department of Environmental Biotechnology, KRIBB School of BiotechnologyUniversity of Science and Technology (UST)DaejeonRepublic of Korea
  3. 3.LED Agri-bio Fusion Technology Research CenterChonbuk National UniversityIksan-siRepublic of Korea

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