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Evaluation of Nutrient Removal and Biomass Production Through Mixotrophic, Heterotrophic, and Photoautotrophic Cultivation of Chlorella in Nitrate and Ammonium Wastewater

  • Azadeh Babaei
  • Mohammad Reza Mehrnia
  • Jalal Shayegan
  • Mohammad-Hossein Sarrafzadeh
  • Elham Amini
Research paper

Abstract

In this study, the effect of mixotrophic, heterotrophic, photoautotrophic (CO2 of air source), and photoautotrophic (bicarbonate source) cultivation of Chlorella vulgaris was investigated on microalgae growth rate and nutrient removal under different kinds of nitrogen sources. The highest N–NH3+, N–NO3, P–PO43− (in ammonium source), and P–PO43− (in nitrate source) removal efficiency (87.28 ± 0.89, 70.00 ± 1.20, 87.00 ± 3.10, and 78.10 ± 1.95%, respectively) was reached in the mixotrophic culture. In all cultivations, when nitrate was used as the nitrogen source, specific growth rate, biomass productivity, and specific oxygen production rate (SOPR) were higher than the one with ammonium source due to decreased pH. However, in all cultures except for photoautotrophic cultivation (in the CO2 of the air), nitrogen removal rates improved in the ammonium source. In addition, in both ammonium and nitrate source, the respiration activity of mixotrophic microalgae was higher than the photosynthetic activity of the cells. When CO2 was used as inorganic carbon, the specific growth rate of microalgae was lower than with the bicarbonate source. Based on the obtained results, mixotrophic conditions would be the most useful cultivation for application in N-rich wastewater treatment systems.

Keywords

Chlorella vulgaris Heterotrophic Mixotrophic Nutrient removal Photoautotrophic 

Notes

Acknowledgements

The authors are grateful to the University of Tehran for supporting this research. In addition, this research was financially supported by Grant No. 11.68722 from the Vice-Presidency for Science and Technology (Presidency of the Islamic Republic of Iran) and the Tehran Province Water and Wastewater Company.

References

  1. Ahmad I, Hellebust J (1984) Nitrogen metabolism of the marine microalgae Chlorella autotrophica. Plant Physiol 76(3):658–663CrossRefGoogle Scholar
  2. Anthonisen AC, Loehr RC, Prakasam TBS, Srinath EG (1976) Inhibition of nitrification by ammonia and nitrous acid. J Water Pollut Contr Fed 48:835–852Google Scholar
  3. APHA (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, NewYorkGoogle Scholar
  4. Aslan S, Kapdan I (2006) Batch kinetics of nitrogen and phosphorus removal from synthetic wastewater by algae. Ecol Eng 28(1):64–70CrossRefGoogle Scholar
  5. Azov Y, Goldman JC (1982) Free ammonia inhibition of algal photosynthesis in intensitive cultures. Appl Environ Microbiol 43(4):735–739Google Scholar
  6. Babaei A, Mehrnia MH, Shayegan J, Sarrafzadeh MH (2016) Comparison of different trophic cultivations in microalgal membrane bioreactor containing N-riched wastewater for simultaneous nutrient removal and biomass production. Process Biochem 51:1568–1575CrossRefGoogle Scholar
  7. Borowitzka MA (1988) Algal growth media and sources of algal cultures. In: Borowitzka MA, Borowitzka LJ (eds) Microalgal biotechnology. Cambridge University Press, Cambridge, pp 456–465Google Scholar
  8. Chen GQ, Chen F (2006) Growing phototrophic cells without light. Biotechnol Lett 28:607–616CrossRefGoogle Scholar
  9. Chen F, Johns MR (1991) Effect of C/N ratio and aeration on fatty acid composition of heterotrophic Chlorella sorokiniana. J Appl Phycol 3:203–209CrossRefGoogle Scholar
  10. Di Caprio F, Altimari P, Pagnanelli F (2015) Integrated biomass production and biodegradation of olive mill wastewater by cultivation of Scenedesmus sp. Algal Res 9:306–311CrossRefGoogle Scholar
  11. Dubey KK, Kumar S, Dixit D, Kumar P, Kumar D, Jawed A, Haque S (2015) Implication of industrial waste for biomass and lipid production in Chlorella minutissima under autotrophic, heterotrophic, and mixotrophic grown conditions. Appl Biochem Biotechnol 176(6):1581–1595CrossRefGoogle Scholar
  12. Fenton O, O hUallachain D (2012) Agricultural nutrient surpluses as potential input sources to grow third generation biomass (microalgae): a review. Algal Res 1:49–56CrossRefGoogle Scholar
  13. Flynn KJ (1991) Algal carbon–nitrogen metabolism: a biochemical basis for modeling the interactions between nitrate and ammonium uptake. J Plankton Res 13(2):373–387CrossRefGoogle Scholar
  14. Ge SH, Champagne P (2016) Nutrient removal, microalgal biomass growth, harvesting and lipid yield in response to centrate wastewater loadings. Water Res 88:604–612CrossRefGoogle Scholar
  15. Goldman JC (1976) Phytoplankton response to wastewater nutrient enrichment in continuous culture. J Exp Mar Biol Ecol 23(1):31–43CrossRefGoogle Scholar
  16. Jalal KCA, Zahangir Alam MD, Matin WA, Kamaruzzaman BY, Akbar J, Toffazel H (2011) Removal of nitrate and phosphate from municipal wastewater sludge by Chlorella vulgaris, Spirulina platensis and Scenedesmus quadricauda. IIUM Eng J 12(4):125–132Google Scholar
  17. Ji MK, Kim HC, Sapireddy VR, Yun HS, Abou-Shanab RA, Choi J, Lee W, Timmes TC, Jeon BH (2013) Simultaneous nutrient removal and lipid production from pretreated piggery wastewater by Chlorella vulgaris YSW-04. Appl Microbiol Biotechnol 97(6):2701–2710CrossRefGoogle Scholar
  18. Kallqvist T, Svenson A (2003) Assessment of ammonia toxicity in tests with the microalgae, Nephroselmis pyriformis, Chlorophyta. Water Res 37(3):477–484CrossRefGoogle Scholar
  19. Kandimalla P, Desi S, Vurimindi H (2016) Mixotrophic cultivation of microalgae using industrial flue gases for biodiesel production. Environ Sci Pollut Res 23:9345–9354CrossRefGoogle Scholar
  20. Kang R, Wang J, Shi D, Cong W, Cai Z, Ouyang F (2004) Interactions between organic and inorganic carbon sources during mixotrophic cultivation of Synechococcus sp. Biotechnol Lett 26(18):1429–1432CrossRefGoogle Scholar
  21. Kim J, Lingaraju BP, Rheaume R, Lee JY, Siddiqui KF (2010) Removal of ammonia from wastewater effluent by Chlorella Vulgaris. Tsinghua Sci Technol 15(4):391–396CrossRefGoogle Scholar
  22. Kim S, Park JE, Cho YB, Hwang SJ (2013a) Growth rate, organic carbon and nutrient removal rates of Chlorella sorokiniana in autotrophic, heterotrophic and mixotrophic conditions. Bioresour Technol 144:8–13CrossRefGoogle Scholar
  23. Kim S, Lee Y, Hwang SJ (2013b) Removal of nitrogen and phosphorus by Chlorella sorokiniana cultured heterotrophically in ammonia and nitrate. Int Biodeter Biodegr 85:511–516CrossRefGoogle Scholar
  24. Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31(7):1043–1049CrossRefGoogle Scholar
  25. Lika K, Papadakis IA (2009) Modeling the biodegradation of phenolic compounds by microalgae. J Sea Res 62(2):135–146CrossRefGoogle Scholar
  26. Lin TS, Wu JY (2015) Effect of carbon sources on growth and lipid accumulation of newly isolated microalgae cultured under mixotrophic condition. Bioresour Technol 184:100–107CrossRefGoogle Scholar
  27. Lowrey J, Brooks MS, McGinn PJ (2015) Heterotrophic and mixotrophic cultivation of microalgae for biodiesel production in agricultural wastewaters and associated challenges—a critical review. J Appl Phycol 27:1485–1498CrossRefGoogle Scholar
  28. Madadi R, Pourbabaee AA, Tabatabaei M, Zahed MA, Naghavi MR (2016) Treatment of petrochemical wastewater by the green algae Chlorella Vulgaris. Int J Environ Res 10(4):555–560Google Scholar
  29. Markou G, Vandamme D, Muylaert K (2014) Microalgal and cyanobacterial cultivation: the supply of nutrients. Water Res 65:186–202CrossRefGoogle Scholar
  30. Marquez FJ, Sasaki K, Kakizono T, Nishio N, Nagai S (1993) Growth characteristics of Spirulina platensis in mixotrophic and heterotrophic conditions. J Ferment Bioeng 76(5):408–410CrossRefGoogle Scholar
  31. Martinez ME, Sánchez S, Jiménez JM, Yousfi F, Muñoz L (2000) Nitrogen and phosphorus removal from urban wastewater by the microalga Scenedesmus obliquus. Bioresour Technol 73(3):263–272CrossRefGoogle Scholar
  32. Min M, Hu B, Zhou W, Li Y, Chen P, Ruan R (2012) Mutual influence of light and CO2 on carbon sequestration via cultivating mixotrophic alga Auxenochlorella protothecoides UMN280 in an organic carbon-rich wastewater. J Appl Phycol 24(5):1099–1105CrossRefGoogle Scholar
  33. Pagnanelli F, Altimari P, Trabucco F, Toro L (2014) Mixotrophic growth of Chlorella vulgaris and Nannochloropsis oculata: interaction between glucose and nitrate. J Chem Technol Biotechnol 89(5):652–661CrossRefGoogle Scholar
  34. Perez-Garcia O, De-Bashan LE, Hernandez JP, Bashan Y (2010) Efficiency of growth and nutrient uptake from wastewater by heterotrophic, autotrophic, and mixotrophic cultivation of Chlorella vulgaris immobilized with Azospirillum brasilense. J Phycol 46(4):800–812CrossRefGoogle Scholar
  35. Perez-Garcia O, Escalante FME, de-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36CrossRefGoogle Scholar
  36. Pourasgharian F, Mehrnia MR, Asadi A, Moayedi Z, Ranjbar R (2014) Effect of microalgae/activated sludge ratio on cooperative treatment of anaerobic effluent of municipal wastewater. Appl Biochem Biotechnol 172:131–140CrossRefGoogle Scholar
  37. Rodrigues MS, Ferreira LS, Converti A, Sato S, Cavalho JC (2010) Fed-batch cultivation of Arthrospira (Spirulina) platensis: potassium nitrate and ammonium chloride as simultaneous nitrogen sources. Bioresour Technol 101(12):4491–4498CrossRefGoogle Scholar
  38. Shi XM, Zhang XW, Chen F (2000) Heterotrophic production of biomass and lutein by Chlorella protothecoides on various nitrogen sources. Enzyme Microb Tech 27(3):312–318CrossRefGoogle Scholar
  39. Shi J, Podola B, Melkonian M (2007) Removal of nitrogen and phosphorus from wastewater using microalgae immobilized on twin layers: an experimental study. J Appl Phycol 19:417–423CrossRefGoogle Scholar
  40. Terry KL, Raymond LP (1985) System design for the autotrophic production of microalgae. Enzyme Microb Tech 7(10):474–487CrossRefGoogle Scholar
  41. Velasco PJ, Tischner R, Huffaker RC, Whitaker JR (1989) Synthesis and degradation of nitrate reductase during the cell cycle of Chlorella sorokiniana. Plant Physiol 89:220–224CrossRefGoogle Scholar
  42. Yeesang C, Cheirsilp B (2014) Low cost production of green microalga Botryococcus braunii biomass with high lipid content through mixotrophic and photoautotrophic cultivation. Appl Biochem Biotechnol 174:116–129CrossRefGoogle Scholar
  43. Zheng Y, Chi Z, Lucker B, Chen S (2012) Two stage heterotrophic and phototrophic culture strategy for algal biomass and lipid production. Bioresour Technol 103(1):484–488CrossRefGoogle Scholar

Copyright information

© University of Tehran 2018

Authors and Affiliations

  • Azadeh Babaei
    • 1
  • Mohammad Reza Mehrnia
    • 1
  • Jalal Shayegan
    • 2
  • Mohammad-Hossein Sarrafzadeh
    • 1
  • Elham Amini
    • 2
  1. 1.School of Chemical Engineering, College of EngineeringUniversity of TehranTehranIran
  2. 2.Department of Chemical and Petroleum EngineeringSharif University of TechnologyTehranIran

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