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Applied Biochemistry and Biotechnology

, Volume 184, Issue 4, pp 1247–1262 | Cite as

Growth of Cyanobacteria: Optimization for Increased Carbohydrate Content

  • Deepika Kushwaha
  • S. N. Upadhyay
  • Pradeep Kumar Mishra
Article

Abstract

Growths of Lyngbya limnetica and Oscillatoria obscura were investigated at varying pH, light intensity, temperature, and trace element concentration with a view to optimize these parameters for obtaining the maximum carbohydrate content. The maximum growth for both strains was obtained at pH 9.0 and temperature 20 ± 3 °C using a light intensity of 68.0 μmol m−2 s−1 with continuous shaking. Growth under the nitrogen starvation condition affected the carbohydrate content more compared to the phosphorus starvation, and maximum concentrations were found as 0.660 and 0.621 g/g of dry biomass for L. limnetica and O. obscura, respectively. Under the optimized nitrogen-rich conditions, the specific growth rates for the two strains were found to be 0.187 and 0.215 day−1, respectively. The two-stage growth studies under nitrogen-rich (stage I) followed by nitrogen starvation (stage II) conditions were performed, and maximum biomass and carbohydrate productivity were found as 0.088 and 0.423 g L−1 day−1 for L. limnetica. This is the first ever attempt to evaluate and optimize various parameters affecting the growth of cyanobacterial biomass of L. limnetica and O. obscura as well as their carbohydrate contents.

Keywords

Cyanobacteria Growth optimization Carbohydrate Specific growth rate Lyngbya limnetica Oscillatoria obscura 

Notes

Acknowledgements

The authors would like to acknowledge the Indian Institute of Technology (BHU) Varanasi for providing the research facilities and the Botanical Survey of India, Kolkata, for identification of cyanobacterial strains.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that there is no conflict of interest.

Supplementary material

12010_2017_2620_MOESM1_ESM.docx (1.6 mb)
ESM 1 (DOCX 1613 kb)

References

  1. 1.
    Demirbas, A. (2010). Social, economic, environmental and policy aspects of biofuels. Energy Education Science and Technology, 2, 75–109.Google Scholar
  2. 2.
    Daroch, M., Geng, S., & Wang, G. (2013). Recent advances in liquid biofuel production from algal feedstocks. Applied Energy, 102, 1371–1381.CrossRefGoogle Scholar
  3. 3.
    Ullah, K., Ahmad, M., Sofia, Sharma, V. K., Lu, P., Harvey, A., Zafar, M., & Sultana, S. (2015). Assessing the potential of algal biomass opportunities for bioenergy industry: a review. Fuel, 143, 414–423.CrossRefGoogle Scholar
  4. 4.
    Graham, J., Wilcox, L., & Graham, L. (2009). Algae (2nd ed.). San Francisco: Benjamin Cummings (Pearson).Google Scholar
  5. 5.
    Kushwaha, D., Saha, S., & Dutta, S. (2014). Enhanced biomass recovery during phycoremediation of Cr(VI) using cyanobacteria and prospect of biofuel production. Industrial & Engineering Chemistry Research, 53, 19754–19764.CrossRefGoogle Scholar
  6. 6.
    Abed, R. M. M., Dobretsov, S., & Sudesh, K. (2009). Applications of cyanobacteria in biotechnology. Journal of Applied Microbiology, 106, 1–12.CrossRefGoogle Scholar
  7. 7.
    Markou, G., Angelidaki, I., Nerantzis, E., & Georgakakis, D. (2013). Bioethanol production by carbohydrate-enriched biomass of Arthrospira (Spirulina) platensis. Energies, 6, 3937–3950.CrossRefGoogle Scholar
  8. 8.
    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.CrossRefGoogle Scholar
  9. 9.
    Xue, C., Zhao, X. Q., Liu, C. G., Chen, L. J., & Bai, F. W. (2013). Prospective and development of butanol as an advanced biofuel. Biotechnology Advances, 31, 1575–1584.CrossRefGoogle Scholar
  10. 10.
    Silva, C. E. F., & Bertucco, A. (2016). Bioethanol from microalgae and cyanobacteria: a review and technological outlook. Process Biochemistry, 51, 1833–1842.CrossRefGoogle Scholar
  11. 11.
    Carvalho, A. P., Monteiro, C. M., & Malcata, F. X. (2009). Simultaneous effect of irradiance and temperature on biochemical composition of the microalga Pavlovalutheri. Journal of Applied Phycology, 21(5), 543–552.CrossRefGoogle Scholar
  12. 12.
    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.CrossRefGoogle Scholar
  13. 13.
    Gonzalez-Fernandez, C., & Ballesteros, M. (2012). Linking microalgae and cyanobacteria culture conditions and key-enzymes for carbohydrate accumulation. Biotechnology Advances, 30, 1655–1661.CrossRefGoogle Scholar
  14. 14.
    Zhang, D., Dechatiwongse, P., del Rio-Chanona, E. A., Maitland, G. C., Hellgardt, K., & Vassiliadis, V. S. (2015). Modelling of light and temperature influences on cyanobacterial growth and biohydrogen production. Algal Research, 9, 263–274.CrossRefGoogle Scholar
  15. 15.
    Tadros, M. G., Smith, W., Joseph, B., & Phillips, J. (1993). Yield and quality of cyanobacteria. Applied Biochemistry and Biotechnology, 39, 337–347.CrossRefGoogle Scholar
  16. 16.
    Carneiro, R. L., Santos, M. E. V. D., Pacheco, A. B. F., & Azevedo, S. M. F. O. (2009). Effects of light intensity and light quality on growth and circadian rhythm of saxitoxins production in Cylindrospermopsis raciborskii (Cyanobacteria). Journal of Plankton Research, 31(5), 481–488.CrossRefGoogle Scholar
  17. 17.
    Ge, H., Zhang, J., Zhou, X., Xia, L., & Hu, C. (2014). Effects of light intensity on components and topographical structure of extracellular polymeric substances from Microcoleus vaginatus (Cyanophyceae). Phycologia, 53(2), 167–173.CrossRefGoogle Scholar
  18. 18.
    Csavina, J. L., Stuart, B. J., Riefler, R. G., & Vis, M. L. (2011). Growth optimization of algae for biodiesel production. Journal of Applied Microbiology, 111, 312–318.CrossRefGoogle Scholar
  19. 19.
    Efremenko, E. N., Nikolskaya, A. B., Lyagin, I. V., Senko, O. V., Makhlis, T. A., Stepanov, N. A., Maslova, O. V., Mamedova, F., & Varfolomeev, S. D. (2012). Production of biofuels from pretreated microalgae biomass by anaerobic fermentation with immobilized Clostridium acetobutylicum cells. Bioresource Technology, 114, 342–348.CrossRefGoogle Scholar
  20. 20.
    Minhas, A. K., Hodgson, P., Barrow, C. J., & Adholeya, A. (2016). A review on the assessment of stress conditions for simultaneous production of microalgal lipids and carotenoids. Frontiers in Microbiology, 7, 546.  https://doi.org/10.3389/fmicb.2016.00546.CrossRefGoogle Scholar
  21. 21.
    Hickman, J. W., Kotovic, K. M., Miller, C., Warrener, P., Kaiser, B., Jurista, T., Budde, M., Cross, F., Roberts, J. M., & Carleton, M. (2013). Glycogen synthesis is a required component of the nitrogen stress response in Synechococcus elongates PCC 7942. Algal Research, 2(2), 98–106.CrossRefGoogle Scholar
  22. 22.
    Xu, Y., & Boeing, W. J. (2014). Modeling maximum lipid productivity of microalgae: review and next step. Renewable and Sustainable Energy Reviews, 32, 29–39.CrossRefGoogle Scholar
  23. 23.
    Mollers, K. B., Cannella, D., Jorgensen, H., & Frigaard, N. U. (2014). Cyanobacterial biomass as carbohydrate and nutrient feedstock for bioethanol production by yeast fermentation. Biotechnology for Biofuels, 7(64), 1–11.Google Scholar
  24. 24.
    Kim, G., Bae, J., & Lee, K. (2016). Nitrate repletion strategy for enhancing lipid production from marine microalga Tetraselmis sp. Bioresource Technology, 205, 274–279.CrossRefGoogle Scholar
  25. 25.
    Kirrolia, A., Bishnoi, N. R., & Singh, R. (2012). Effect of shaking, incubation temperature, salinity and media composition on growth traits of green microalgae Chlorococcum sp. Journal of Algal Biomass Utilization, 3(3), 46–53.Google Scholar
  26. 26.
    Rotatore, C., & Colman, B. (1991). The acquisition and accumulation of inorganic carbon by the unicellular green alga Chlorella ellipsoidea. Plant, Cell & Environment, 14, 377–382.CrossRefGoogle Scholar
  27. 27.
    Bartley, M. L., Boeing, W. J., Dungan, B. N., Holguin, F. O., & Schaub, T. (2014). pH effect on growth and lipid accumulation of the biofuel microalgae Nannochloropsis salina and invading organisms. Journal of Applied Phycology, 26, 1431–1437.CrossRefGoogle Scholar
  28. 28.
    Li, Y., Lin, Y., Loughlin, P. C., & Chen, M. (2014). Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris—a filamentous cyanobacterium containing chlorophyll f. Frontiers in Plant Science, 5, 1–12.  https://doi.org/10.3389/fpls.2014.00067.Google Scholar
  29. 29.
    Silva, C. E. F., Sforza, E., & Bertucco, A. (2017). Effect of pH and carbon source on Synechococcus PCC 7002 cultivation: biomass and carbohydrate production with different strategies for pH control. Applied Biochemistry and Biotechnology, 181, 682–698.CrossRefGoogle Scholar
  30. 30.
    Silva, C. E. F., Gris, B., Sforza, E., La Rocca, N., & Bertucco, A. (2016). Effects of sodium bicarbonate on biomass and carbohydrate production in Synechococcus PCC 7002. Chemical Engineering Transactions, 49, 241–246.Google Scholar
  31. 31.
    Mackey, K. R. M., Paytan, A., Caldeira, K., Grossman, A. R., Moran, D., Mcllvin, M., & Saito, M. A. (2013). Effect of temperature on photosynthesis and growth in marine Synechococcus spp. Plant Physiology, 163(2), 815–829.CrossRefGoogle Scholar
  32. 32.
    Converti, A., Casazza, A. A., Ortiz, E. Y., Perego, P., & Borghi, M. D. (2009). Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chemical Engineering and Processing, 48(6), 1146–1151.CrossRefGoogle Scholar
  33. 33.
    Demeter, S., Janda, T., Kovacs, L., Mende, D., & Wiessner, W. (1995). Effects of in vivo CO2-depletion on electron transport and photoinhibition in the green algae, Chlamydobotrys stellata and Chlamydomonas reinhardtii. Biochimica et Biophysica Acta, 1229, 166–174.CrossRefGoogle Scholar
  34. 34.
    Kumar, K., & Das, D. (2014). Carbon dioxide sequestration by biological processes. In B. M. Bhanage & M. Arai (Eds.), Transformation and utilization of carbon dioxide (pp. 303–334). Heidelberg: Springer.CrossRefGoogle Scholar
  35. 35.
    Dyble, J., Tester, P. A., & Litaker, R. W. (2006). Effects of light intensity on cylindrospermopsin production in the cyanobacterial HAB species Cylindrospermopsis raciborskii. African Journal of Marine Science, 28(2), 309–312.CrossRefGoogle Scholar
  36. 36.
    Chow, T., Su, H., Tsai, T., Chou, H., Lee, T., & Chang, J. (2015). Using recombinant cyanobacterium (Synechococcus elongates) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process. Bioresource Technology, 184, 33–41.CrossRefGoogle Scholar
  37. 37.
    Vitova, M., Bisova, K., Kawano, S., & Zachleder, V. (2015). Accumulation of energy reserves in algae: From cell cycles to biotechnological applications. Biotechnology Advances, 33, 1204–1218.CrossRefGoogle Scholar
  38. 38.
    Singh, S. P., & Singh, P. (2015). Effect of temperature and light on the growth of algae species: a review. Renewable and Sustainable Energy Reviews, 50, 431–444.CrossRefGoogle Scholar
  39. 39.
    Khajepour, F., Hosseini, S. A., Nasrabadi, R. G., & Markou, G. (2015). Effect of light intensity and photoperiod on growth and biochemical composition of a local isolate of Nostoc calcicola. Applied Biochemistry and Biotechnology, 176, 2279–2289.CrossRefGoogle Scholar
  40. 40.
    Dammak, M., Hadrich, B., Miladi, R., Barkallah, M., Hentati, F., Hachicha, R., Laroche, C., Michaud, P., Fendri, I., & Abdelkafi, S. (2017). Effects of nutritional conditions on growth and biochemical composition of Tetraselmis sp. Lipids in Health and Disease, 16(1), 41.  https://doi.org/10.1186/s12944-016-0378-1.CrossRefGoogle Scholar
  41. 41.
    Depraetere, O., Deschoenmaeker, F., Badri, H., Monsieurs, P., Foubert, I., Leys, N., Wattiez, R., & Muylaert, K. (2015). Trade-off between growth and carbohydrate accumulation in nutrient-limited Arthrospira sp. PCC 8005 studied by integrating transcriptomic and proteomic approaches. PLoS One, 10(7), e0132461.  https://doi.org/10.1371/journal.pone.0132461.CrossRefGoogle Scholar
  42. 42.
    Taraldsvik, M., & Myklestad, S. (2000). The effect of pH on growth rate, biochemical composition and extracellular carbohydrate production of the marine diatom Skeletonema costatum. European Journal of Phycology, 35(2), 189–194.CrossRefGoogle Scholar
  43. 43.
    Sun, X., Cao, Y., Xu, H., Liu, Y., Sun, J., Qiao, D., & Cao, Y. (2014). Effect of nitrogen-starvation, light intensity and iron on triacylglyceride/carbohydrate production and fatty acid profile of Neochloris oleoabundans HK-129 by a two-stage process. Bioresource Technology, 155, 204–212.CrossRefGoogle Scholar
  44. 44.
    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, 3331–3335.CrossRefGoogle Scholar
  45. 45.
    Hasunuma, T., Kikuyama, F., Matsuda, M., Aikawa, S., Izumi, Y., & Kondo, A. (2013). Dynamic metabolic profiling of cyanobacterial glycogen biosynthesis under conditions of nitrate depletion. Journal of Experimental Botany, 64, 2943–2954.CrossRefGoogle Scholar
  46. 46.
    Aikawa, S., Nishida, A., Ho, S. H., Chang, J. S., Hasunuma, T., & Kondo, A. (2014). Glycogen production for biofuels by the euryhaline cyanobacteria Synechococcus sp. strain PCC 7002 from an oceanic environment. Biotechnology for Biofuels, 7(1), 88.CrossRefGoogle Scholar
  47. 47.
    Mendez, L., Mahdy, A., Ballesteros, M., & Gonzalez-Fernandez, C. (2015). Chlorella vulgaris vs cyanobacterial biomasses: comparison in terms of biomass productivity and biogas yield. Energy Conversion and Management, 92, 137–142.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Deepika Kushwaha
    • 1
  • S. N. Upadhyay
    • 1
  • Pradeep Kumar Mishra
    • 1
  1. 1.Department of Chemical Engineering & TechnologyIndian Institute of Technology (BHU) VaranasiVaranasiIndia

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