Skip to main content

Advertisement

SpringerLink
Log in

Enhanced Accumulation of Carbohydrate and Starch in Chlorella zofingiensis Induced by Nitrogen Starvation

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Though less attention has been paid to microalgae as a feedstock for bioethanol production, many microalgae seem to have this potential since they contain no lignin, minor hemicellulose, and abundant carbohydrate. The objective of this study was to investigate the effect of nitrogen starvation on carbohydrate and starch accumulation in green microalga Chlorella zofingiensis and assess the feasibility of using this microalga as a bioethanol feedstock. The results showed that the specific growth rate under nitrogen starvation (0.48 day−1) was much lower than that under nitrogen repletion (1.02 day−1). However, nitrogen starvation quickly induced the accumulation of carbohydrate, especially starch. After merely 1 day of nitrogen starvation, carbohydrate and starch increased 37 % and 4.7-fold, respectively. The highest carbohydrate content reached 66.9 % of dry weight (DW), and 66.7 % of this was starch. In order to obtain enough carbohydrate productivities for bioethanol production, two-stage cultivation strategy was implemented and found to be effective for enhancing biomass, carbohydrate, and starch simultaneously. The optimal biomass, carbohydrate, and starch productivities of C. zofingiensis were obtained after 5 days of cultivation, and their values were 699, 407, and 268 mg L−1 day−1, respectively.

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

Similar content being viewed by others

References

  1. Dragone, G., Fernandes, B. D., Abreu, A. P., Vicente, A. A., & Teixeira, J. A. (2011). Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Applied Energy, 88(10), 3331–3335.

    Article  CAS  Google Scholar 

  2. Doan, Q. C., Moheimani, N. R., Mastrangelo, A. J., & Lewis, D. M. (2012). Microalgal biomass for bioethanol fermentation: implications for hypersaline systems with an industrial focus. Biomass and Bioenergy, 46, 79–88.

    Article  CAS  Google Scholar 

  3. Sun, Y., & Cheng, J. Y. (2002). Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresource Technology, 83, 1–11.

    Article  CAS  Google Scholar 

  4. Chen, C. Y., Zhao, X. Q., Yen, H. W., Ho, S. H., Cheng, C. L., Lee, D. J., Bai, F. W., & Chang, J. S. (2013). Microalgae-based carbohydrates for biofuel production. Biochemical Engineering Journal, 78, 1–10.

    Article  CAS  Google Scholar 

  5. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., & Darzins, A. (2008). Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant Journal, 54(4), 621–639.

    Article  CAS  Google Scholar 

  6. Wijffels, R. H., & Barbosa, M. J. (2010). An outlook on microalgal biofuels. Science, 329(5993), 796–799.

    Article  CAS  Google Scholar 

  7. Ho, S. H., Huang, S. W., Chen, C. Y., Hasunuma, T., Kondo, A., & Chang, J. S. (2013). Characterization and optimization of carbohydrate production from an indigenous microalga Chlorella vulgaris FSP-E. Bioresource Technology, 135, 157–165.

    Article  CAS  Google Scholar 

  8. Markou, G., Angelidaki, I., & Georgakakis, D. (2012). Microalgal carbohydrates: an overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Applied Microbiology and Biotechnology, 96(3), 631–645.

    Article  CAS  Google Scholar 

  9. Choix, F. J., de Bashan, L. E., & Bashan, Y. (2012). Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense: I. Autotrophic conditions. Enzyme and Microbial Technology, 51(5), 294–299.

    Article  CAS  Google Scholar 

  10. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28(3), 350–356.

    Article  CAS  Google Scholar 

  11. Branyikova, I., Marsalkova, B., Doucha, J., Branyik, T., Bisova, K., Zachleder, V., & Vitova, M. (2011). Microalgae-novel highly efficient starch producers. Biotechnology and Bioengineering, 108(4), 766–776.

    Article  CAS  Google Scholar 

  12. Recht, L., Zarka, A., & Boussiba, S. (2012). Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Applied Microbiology and Biotechnology, 94(6), 1495–1503.

    Article  CAS  Google Scholar 

  13. Lv, J. M., Cheng, L. H., Xu, X. H., Zhang, L., & Chen, H. L. (2010). Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresource Technology, 101, 6797–6804.

    Article  CAS  Google Scholar 

  14. Wang, L., Li, Y. G., Sommerfeld, M., & Hu, Q. (2013). A flexible culture process for production of the green microalga Scenedesmus dimorphus rich in protein, carbohydrate or lipid. Bioresource Technology, 129, 289–295.

    Article  CAS  Google Scholar 

  15. González-Fernández, C., & Ballesteros, M. (2012). Linking microalgae and cyanobacteria culture conditions and key-enzymes for carbohydrate accumulation. Biotechnology Advances, 30(6), 1655–1661.

    Article  Google Scholar 

  16. Roessler, P. G. (1987). Udpglucose pyrophosphorylase activity in the diatom Cyclotella cryptica—pathway of chrysolaminarin biosynthesis. Journal of Phycology, 23(3), 494–498.

    Article  CAS  Google Scholar 

  17. Yao, C., Ai, J., Cao, X., Xue, S., & Zhang, W. (2012). Enhancing starch production of a marine green microalga Tetraselmis subcordiformis through nutrient limitation. Bioresource Technology, 118, 438–444.

    Article  CAS  Google Scholar 

  18. Fan, J. L., Yan, C. S., Andre, C., Shanklin, J., Schwender, J., & Xu, C. C. (2012). Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant and Cell Physiology, 53(8), 1380–1390.

    Article  CAS  Google Scholar 

  19. Zhu, S., Huang, W., Xu, J., Wang, Z., Xu, J., & Yuan, Z. (2014). Metabolic changes of starch and lipid triggered by nitrogen starvation in the microalga Chlorella zofingiensis. Bioresource Technology, 152, 292–298.

    Article  CAS  Google Scholar 

  20. Li, Y. T., Han, D. X., Sommerfeld, M., & Hu, Q. (2011). Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions. Bioresource Technology, 102, 123–129.

    Article  CAS  Google Scholar 

  21. Wan, L. L., Han, J., Sang, M., Li, A. F., Wu, H., Yin, S. J., & Zhang, C. W. (2012). De novo transcriptomic analysis of an oleaginous microalga: pathway description and gene discovery for production of next-generation biofuels. Plos One, 7, e35142.

    Article  CAS  Google Scholar 

  22. Foy, R. H., & Smith, R. V. (1980). The role of carbohydrate accumulation in the growth of planktonic Oscillatoria species. British Phycological Journal, 15(2), 139–150.

    Article  Google Scholar 

  23. Ballicora, M., Iglesias, A., & Preiss, J. (2004). ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynthesis Research, 79(1), 1–24.

    Article  CAS  Google Scholar 

  24. Rodolfi, L., Zittelli, G. C., Bassi, N., Padovani, G., Biondi, N., Bonini, G., & Tredici, M. R. (2009). Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnology and Bioengineering, 102(1), 100–112.

    Article  CAS  Google Scholar 

  25. Ho, S. H., Chen, W. M., & Chang, J. S. (2010). Scenedesmus obliquus CNW-N as a potential candidate for CO2 mitigation and biodiesel production. Bioresource Technology, 101, 8725–8730.

    Article  CAS  Google Scholar 

  26. Han, D. X., Li, Y. T., & Hu, Q. (2013). Astaxanthin in microalgae: pathways, functions and biotechnological implications. Algae, 28(2), 131–147.

    Article  CAS  Google Scholar 

  27. Ho, S. H., Li, P. J., Liu, C. C., & Chang, J. S. (2013). Bioprocess development on microalgae-based CO2 fixation and bioethanol production using Scenedesmus obliquus CNW-N. Bioresource Technology, 145, 142–149.

    Article  CAS  Google Scholar 

  28. Griffiths, M. J., & Harrison, S. T. L. (2009). Lipid productivity as a key characteristic for choosing algal species for biodiesel production. Journal of Applied Phycology, 21(5), 493–507.

    Article  CAS  Google Scholar 

  29. Ho, S. H., Chen, C. Y., & Chang, J. S. (2012). Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresource Technology, 113, 244–252.

    Article  CAS  Google Scholar 

  30. Yao, C. H., Ai, J. N., Cao, X. P., & Xue, S. (2013). Characterization of cell growth and starch production in the marine green microalga Tetraselmis subcordiformis under extracellular phosphorus-deprived and sequentially phosphorus-replete conditions. Applied Microbiology and Biotechnology, 97(13), 6099–6110.

    Article  CAS  Google Scholar 

  31. Sassano, C. E. N., Gioielli, L. A., Ferreira, L. S., Rodrigues, M. S., Sato, S., Converti, A., & Carvalho, J. C. M. (2010). Evaluation of the composition of continuously-cultivated Arthrospira (Spirulina) platensis using ammonium chloride as nitrogen source. Biomass and Bioenergy, 34(12), 1732–1738.

    Article  CAS  Google Scholar 

  32. De Philippis, R., Sili, C., & Vincenzini, M. (1992). Glycogen and poly-β-hydroxybutyrate synthesis in Spirulina maxima. Journal of General Microbiology, 138(8), 1623–1628.

    Article  Google Scholar 

Download references

Acknowledgments

This research was financially supported by National Natural Science Foundation of China (No. 31100189), the National Basic Research Program of China (973 Program) (2011CB200905), the 12th Five Year Support Plan of the Ministry of Science and Technology, China (2011BAD14B03), National High-tech R&D Program (2013AA065803), and the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry.

Author information

Authors and Affiliations

  1. Guangzhou Institute of Energy Conversion, Chinese Academy of Sciences, Guangzhou, 510640, China

    Shunni Zhu, Yajie Wang, Wei Huang, Jin Xu, Zhongming Wang, Jingliang Xu & Zhenhong Yuan

  2. University of Chinese Academy of Sciences, Beijing, 100039, China

    Yajie Wang & Wei Huang

  3. Key Laboratory of Renewable Energy, Guangzhou Institute of Energy Conversion, Chinese Academy of Sciences, Guangzhou, 510640, China

    Zhenhong Yuan

Authors
  1. Shunni Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yajie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhongming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jingliang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhenhong Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhenhong Yuan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, S., Wang, Y., Huang, W. et al. Enhanced Accumulation of Carbohydrate and Starch in Chlorella zofingiensis Induced by Nitrogen Starvation. Appl Biochem Biotechnol 174, 2435–2445 (2014). https://doi.org/10.1007/s12010-014-1183-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-014-1183-9

Keywords

Search

Navigation