Advertisement

Journal of Applied Phycology

, Volume 31, Issue 2, pp 1001–1008 | Cite as

Exogenous sodium acetate enhances astaxanthin accumulation and photoprotection in Haematococcus pluvialis at the non-motile stage

  • Chunhui Zhang
  • Litao Zhang
  • Jianguo LiuEmail author
Article

Abstract

The purpose of this study was to analyze the effects of exogenous sodium acetate on astaxanthin accumulation and photoprotection in Haematococcus pluvialis at the non-motile stage. Five or 10 mM sodium acetate increased astaxanthin contents more than two-fold as compared with that in cells without sodium acetate after 6 days of incubation, indicating that exogenous sodium acetate accelerated astaxanthin accumulation at the non-motile stage significantly. Addition of sodium acetate inhibited the chlorophyll fluorescence parameters (ΦPSII, Fv′/Fm′, and qL) as well as photosynthetic rates, indicating that exogenous sodium acetate suppressed photosynthetic activity. However, additional sodium acetate increased respiratory rates. It can be speculated that the enhanced respiration plays an important role in the acceleration of astaxanthin accumulation in the presence of sodium acetate, because acetate can be utilized by the respiratory tricarboxylic acid cycle to generate the carbon skeletons and NAD(P)H for astaxanthin synthesis. Moreover, the level of photoinhibition decreased after adding sodium acetate, which is indicated by the fact that the decrease of the Fv/Fm value from predawn to midday declined on day 4 and day 6. NPQ increased significantly with additional sodium acetate on day 4 and day 6, indicating that additional sodium acetate induced a mechanism to protect algal cells against photoinhibition. Taken together, exogenous sodium acetate enhances astaxanthin accumulation and the photoprotection capacity of H. pluvialis at the non-motile stage.

Keywords

Haematococcus pluvialis Exogenous sodium acetate Astaxanthin accumulation Photoprotection Photoinhibition 

Notes

Acknowledgements

We thank Dr. John van der Meer (Pan-American Marine Biotechnology Association) for his English editing.

Contributions

Chunhui Zhang and Jianguo Liu designed the study and wrote the manuscript; Chunhui Zhang and Litao Zhang performed the experiments and analyzed the data. All authors read and approved the manuscript.

Funding information

This work was financial supported by National Natural Science Foundation of China (Nos. 31572639, U1706209).

References

  1. Becker HM, Hirnet D, Fecher-Trost C, Sultemeyer D, Deitmer JW (2005) Transport activity of MCT1 expressed in Xenopus oocytes is increased by interaction with carbonic anhydrase. J Biol Chem 280:39882–39889CrossRefGoogle Scholar
  2. Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185CrossRefGoogle Scholar
  3. Borowitzka MA, Huisman JM, Osborn A (1991) Culture of the astaxanthin-producing green alga Haematococcus pluvialis, 1. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304CrossRefGoogle Scholar
  4. Boyle NR, Morgan JA (2009) Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Systems Biol 3:1–14CrossRefGoogle Scholar
  5. Göksan T, Ak İ, Şevket G (2010) An alternative approach to the traditional mixotrophic cultures of Haematococcus pluvialis Flotow (Chlorophyceae). J Microbiol Biotechnol 20:1276–1282CrossRefGoogle Scholar
  6. Hagen C, Grünewald K, Xyländer M, Rothe E (2001) Effect of cultivation parameters on growth and pigment biosynthesis in flagellated cells of Haematococcus pluvialis. J Appl Phycol 13:79–87CrossRefGoogle Scholar
  7. Hong SJ, Lee CG (2007) Evaluation of central metabolism based on a genomic database of Synechocystis PCC6803. Biotechnol Bioprocess Eng 12:165–173CrossRefGoogle Scholar
  8. Hussein G, Sankawa U, Goto H, Matsumoto K, Watanabe H (2006) Astaxanthin, a carotenoid with potential in human health and nutrition. J Nat Prod 69:443–449CrossRefGoogle Scholar
  9. Jiang CD, Gao HY, Zou Q, Jiang GM, Li LH (2004) Leaf orientation, photorespiration and xanthophyll cycle protect young soybean leaves against high irradiance in field. Env Exp Bot 55:87–96CrossRefGoogle Scholar
  10. Johnson GN, Young AJ, Scholes JD, Horton P (1993) The dissipation of excess excitation energy in British plant species. Plant Cell Environ 16:673–679CrossRefGoogle Scholar
  11. Johnson X, Alric J (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J Biol Chem 287:26445–26452CrossRefGoogle Scholar
  12. Ke J, Behal RH, Back SL, Nikolau BJ (2000) The role of pyruvate dehydrogenase and acetyl-coenzyme A synthetase in fatty acid synthesis in developing Arabidopsis seeds. Plant Physiol 123:497–508CrossRefGoogle Scholar
  13. Kim DK, Hong SJ, Bae JH, Yim N, Jin E, Lee C-G (2011) Transcriptomic analysis of Haematococcus lacustris, during astaxanthin accumulation under high irradiance and nutrient starvation. Biotechnol Bioprocess Eng 16:698–705CrossRefGoogle Scholar
  14. 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 59:867–873Google Scholar
  15. Kobayashi M, Kakizono T, Yamaguchi K, Nishio N, Nagai S (1992) Growth and astaxanthin formation of Haematococcus pluvialis in heterotrophic and mixotrophic conditions. J Ferment Bioeng 74:17–20CrossRefGoogle Scholar
  16. Kobayashi M, Sakamoto Y (1999) Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis. Biotechnol Lett 21:265–269CrossRefGoogle Scholar
  17. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218CrossRefGoogle Scholar
  18. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148:350–382CrossRefGoogle Scholar
  19. Lin M, Oliver DJ (2008) The role of acetyl-coenzyme A synthetase in Arabidopsis. Plant Physiol 147:1822–1829CrossRefGoogle Scholar
  20. Liu JG, Yin MY, Zhang JP, Liu W, Meng ZC (2002) Dynamic changes of inorganic nitrogen and astaxanthin accumulation in Haematococcus pluvialis. Chin J Oceanol Limnol 20:358–364CrossRefGoogle Scholar
  21. Liu JG, Li QQ, Liu Q, He M, Zhang L, Liu YD, Ding Y, Zhang Z, Lin W, Song P, Li L, Huang Y, Han C (2014) Screening of unicellular microalgae for biofuels and bioactive products and development of a pilot platform. Algol Stud 145:99–117CrossRefGoogle Scholar
  22. Masojídek J, Torzillo G, Kopecký J, Koblížek M, Nidiaci L, Komenda A, Lukavska A, Sacchi A (2000) Changes in chlorophyll fluorescence quenching and pigment composition in the green alga Chlorococcum sp. grown under nitrogen deficiency and salinity stress. J Appl Phycol 12:417–426CrossRefGoogle Scholar
  23. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  24. Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460CrossRefGoogle Scholar
  25. Orosa M, Franqueira D, Cid A, Albade J (2001) Carotenoid accumulation in Haematococcus pluvialis in mixotrophic growth. Biotechnol Lett 23:373–378CrossRefGoogle Scholar
  26. Perez-Garcia O, Escalante FM, De-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36CrossRefGoogle Scholar
  27. Scibilia L, Girolomoni L, Berteotti S, Alboresi A, Ballottari M (2015) Photosynthetic response to nitrogen starvation and high light in Haematococcus pluvialis. Algal Res 12:170–181CrossRefGoogle Scholar
  28. Steinbrenner J, Linden H (2000) Regulation of two carotenoid biosynthesis genes coding for phytoene synthase and carotenoid hydroxylase during stress-induced astaxanthin biosynthesis in the green alga Haematococcus pluvialis. Plant Physiol 125:810–817CrossRefGoogle Scholar
  29. Steinbrenner J, Linden H (2003) Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis: regulation by photosynthetic redox control. Plant Molec Biol 52:343–356CrossRefGoogle Scholar
  30. Sun YH, Liu JG, Zhang XL, Lin W (2008) Strain H 2-419-4 of Haematococcus pluvialis induced by ethyl methanesulphonate and ultraviolet radiation. Chin J Oceanol Limnol 26:152–156CrossRefGoogle Scholar
  31. Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149:1560–1567CrossRefGoogle Scholar
  32. Wang N, Guan B, Kong Q, Duan L (2018) A semi-continuous cultivation method for Haematococcus pluvialis from non-motile cells to motile cells. J Appl Phycol 30:773–781CrossRefGoogle Scholar
  33. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Phil Trans Roy Soc B 355:1517–1529CrossRefGoogle Scholar
  34. Yang C, Hua Q, Shimizu K (2000) Energetics and carbon metabolism during growth of microalgal cells under photoautotrophic, mixotrophic and cyclic light-autotrophic/dark-heterotrophic conditions. Biochem Eng J 6:87–102CrossRefGoogle Scholar
  35. Yang C, Hua Q, Shimizu K (2002) Integration of the information from gene expression and metabolic fluxes for the analysis of the regulatory mechanisms in Synechocystis. Appl Microbiol Biotechnol 58:813–822CrossRefGoogle Scholar
  36. Zhang CH, Liu JG, Zhang LT (2017a) Cell cycles and proliferation patterns in Haematococcus pluvialis. Chin J Oceanol Limnol 35:1205–1211CrossRefGoogle Scholar
  37. Zhang CH, Zhang LT, Liu JG (2016b) The role of photorespiration during astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae). Plant Physiol Biochem 107:75–81CrossRefGoogle Scholar
  38. Zhang LT, He ML, Liu JG, Li L (2015) Role of the mitochondrial alternative oxidase pathway in hydrogen photoproduction in Chlorella protothecoides. Planta 241:1005–1014CrossRefGoogle Scholar
  39. Zhang LT, Li L, He ML, Liu J (2016a) The role of photorespiration during H2 photoproduction in Chlorella protothecoides under nitrogen limitation. Plant Cell Rep 35:1–4CrossRefGoogle Scholar
  40. Zhang LT, Su F, Zhang CH, Gong F, Liu J (2017b) Changes of photosynthetic behaviors and photoprotection during cell transformation and astaxanthin accumulation in Haematococcus pluvialis grown outdoors in tubular photobioreactors. Int J Molec Sci 18:33CrossRefGoogle Scholar
  41. Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2011) Mitochondrial alternative oxdiase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Plant 143:396–407CrossRefGoogle Scholar
  42. Zhekisheva M, Boussiba S, Khozin-Goldberg I, 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 eaters. J Phycol 38:325–331CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.CAS Key Laboratory of Experimental Marine Biology, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Laboratory for Marine Biology and BiotechnologyQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.National-Local Joint Engineering Research Center for Haematococcus pluvialis and Astaxanthin ProductsYunnan Alphy Biotech Co., Ltd.ChuxiongChina

Personalised recommendations