Journal of Applied Phycology

, Volume 31, Issue 5, pp 2833–2844 | Cite as

Assimilation of inorganic nitrogen for scaling up Desmodesmus communis (Scenedesmaceae) biomass production

  • Laura PezzolesiEmail author
  • Matilde Mazzotti
  • Silvana Vanucci
  • Rossella Pistocchi


The feasibility of the green alga Desmodesmus communis for biomass production was investigated, firstly testing different nitrogen forms in the growth medium and the effect of CO2-enriched air supply, secondarily scaling up the cultivation system in 70 L photobioreactors (PBRs). Maximum nitrogen uptake rate obtained in the performed kinetic experiment was higher for ammonium than for nitrate (188.0 vs 11.7 μmol g−1 h−1); however, D. communis cultured in PBRs with only aeration grew faster with nitrate reaching a biomass yield (1.23 g L−1) and a productivity (0.036 g L−1 day−1) about twofold higher than with ammonium, which caused a pH decrease in the medium affecting the algal growth. CO2 supply allowed algal growth optimization, maintaining a high productivity with both nitrogen sources, slightly higher with nitrate (0.050 vs 0.038 g L−1 day−1). Additionally, nitrate-supplied cells showed higher lipids (19.0 vs 9.4%) and proteins (33.0 vs 27.2%) values than those grown with ammonium. The semi-continuous scaled-up cultivation performed for 5 months attests the potential utilization of this species for valuable algal biomass production exploitable in various industrial applications.


Desmodesmus Chlorophyta Nitrogen Algal biomass Photobioreactor 



This study was supported by the framework of the APQ Ricerca Intervento a “Sostegno dello sviluppo dei Laboratori di ricerca nei campi della nautica e dell’energia per il Tecnopolo di Ravenna” “Energia, parte Biomasse” between Università di Bologna and Regione Emilia Romagna (Italy). The authors are very grateful to the reviewers for the careful reading of the paper, and their valuable comments and corrections that help to improve the manuscript.

Authors’ contributions

LP and MM did the conception and design of the study and the analysis and interpretation of the data. LP and, partially, MM wrote the article. SV and RP helped in the interpretation of the data. SV did the critical revision of the article for important intellectual content. RS did the final approval of the article and obtained the funding to perform the work. All authors approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


  1. Abe H (1985) Ouyo Sugaku Nyumon. Baifu Kan, Tokyo, p 215 (in Japanese)Google Scholar
  2. APHA (American Public Health Association) (1995) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DCGoogle Scholar
  3. Arumugam M, Agarwal A, Arya MC, Ahmed Z (2013) Influence of nitrogen sources on biomass productivity of microalgae Scenedesmus bijugatus. Bioresour Technol 131:246–249PubMedGoogle Scholar
  4. Aslan S, Kapdan IK (2006) Batch kinetics of nitrogen and phosphorus removal from synthetic wastewater by algae. Ecol Eng 28:64–70Google Scholar
  5. Barbera E, Bertucco A, Kumar S (2018) Nutrients recovery and recycling in algae processing for biofuels production. Renew Sust Energ Rev 90:28–42Google Scholar
  6. Basu S, Roy AS, Ghoshal AK, Mohanty K (2015) Operational strategies for maximizing CO2 utilization efficiency by the novel microalga Scenedesmus obliquus SA1 cultivated in lab scale photobioreactor. Algal Res 12:249–257Google Scholar
  7. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedPubMedCentralGoogle Scholar
  8. Borowitzka MA (2013) Energy from microalgae: a short history. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 1–15Google Scholar
  9. Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14:557–577Google Scholar
  10. Cabello J, Morales M, Revah S (2017) Carbon dioxide consumption of the microalga Scenedesmus obtusiusculus under transient inlet CO2 concentration variations. Sci Total Environ 584–585:1310–1316PubMedGoogle Scholar
  11. Collos Y, Vaquer A, Souchu P (2005) Acclimation of nitrate uptake by phytoplankton to high substrate levels. J Phycol 41:466–478Google Scholar
  12. Conti R, Pezzolesi L, Pistocchi R, Torri C, Massoli P, Fabbri D (2016) Photobioreactor cultivation and catalytic pyrolysis of the microalga Desmodesmus communis (Chlorophyceae) for hydrocarbons production by HZSM-5 zeolite cracking. Bioresour Technol 222:148–155PubMedGoogle Scholar
  13. Eustance E, Gardner RD, Moll KM, Menicucci J, Gerlach R, Peyton BM (2013) Growth, nitrogen utilization and biodiesel potential for two chlorophytes grown on ammonium, nitrate or urea. J Appl Phycol 25:1663–1677Google Scholar
  14. Ferro L, Gentili FG, Funk C (2018) Isolation and characterization of microalgal strains for biomass production and wastewater reclamation in Northern Sweden. Algal Res 32:44–53Google Scholar
  15. Gao F, Li C, Yang ZH, Zeng GM, Feng LJ, Liu JZ, Liu M, Cai HW (2016) Continuous microalgae cultivation in aquaculture wastewater by a membrane photobioreactor for biomass production and nutrients removal. Ecol Eng 92:55–61Google Scholar
  16. Garcia J, Green B, Oswald W (2006) Long term diurnal variations in contaminant removal in high rate ponds treating urban wastewater. Bioresour Technol 97:1709–1715PubMedGoogle Scholar
  17. Ge Y, Liu J, Tian G (2011) Growth characteristics of Botryococcus braunii 765 under high CO2 concentration in photobioreactor. Bioresour Technol 102:130–134PubMedGoogle Scholar
  18. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophya Acta - Gen Subjects 990:87–92Google Scholar
  19. George B, Pancha I, Desai C, Chokshi K, Paliwal C, Ghosh T, Mishra S (2014) Effects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmus falcatus—a potential strain for bio-fuel production. Bioresour Technol 171:367–374PubMedGoogle Scholar
  20. Gour RS, Bairagi M, Garlapati VK, Kant A (2018) Enhanced microalgal lipid production with media engineering of potassium nitrate as a nitrogen source. Bioengineered 9:98–107PubMedGoogle Scholar
  21. Gouveia L, Graça S, Sousa C, Ambrosano L, Ribeiro B, Botrel EP, Neto PC, Ferreira AF, Silva CM (2016) Microalgae biomass production using wastewater: treatment and costs scale-up considerations. Algal Res 16:167–176Google Scholar
  22. Gressler P, Bjerk T, Schneider R, Souza M, Lobo E, Zappe A, Corbellini V, Moraes M (2014) Cultivation of Desmodesmus subspicatus in a tubular photobioreactor for bioremediation and microalgae oil production. Environ Technol 35:209–219PubMedGoogle Scholar
  23. Hughes E, Benemann JR (1997) Biological fossil CO2 mitigation. Energ Convers Manage 38:S467–S473Google Scholar
  24. Hyenstrand P, Burkert U, Pettersson A, Blomqvist P (2000) Competition between the green alga Scenedesmus and the cyanobacterium Synechococcus under different modes of inorganic nitrogen supply. Hydrobiologia 435:91–98Google Scholar
  25. Kochert G (1978) Carbohydrate determination by the phenol-sulfuric acid method. In: Hellebust JA, Craigie JS (eds) Handbook of Phycological Methods: Physiological and Biochemical Methods. Cambridge University Press, London, pp 95–97Google Scholar
  26. Komolafe O, Orta SBV, Monje-Ramirez I, Noguez IY, Harvey AP, Ledesma MTO (2014) Biodiesel production from indigenous microalgae grown in wastewater. Bioresour Technol 154:297–304PubMedGoogle Scholar
  27. Kwon HK, Oh SJ, Yang H-S (2013) Growth and uptake kinetics of nitrate and phosphate by benthic microalgae for phytoremediation of eutrophic coastal sediments. Bioresour Technol 129:387–395PubMedGoogle Scholar
  28. Lim PT, Leaw CP, Usup G, Kobiyama A, Koike K, Ogata T (2006) Effects of light and temperature on growth, nitrate uptake, and toxin production of two tropical dinoflagellates: Alexandrium tamiyavanichii and Alexandrium minutum (Dinophyceae). J Phycol 42:786–799Google Scholar
  29. Lin Q, Lin J (2011) Effects of nitrogen source and concentration on biomass and oil production of a Scenedesmus rubescens like microalga. Bioresour Technol 102:1615–1621PubMedGoogle Scholar
  30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedPubMedCentralGoogle Scholar
  31. Martı́nez ME, Sánchez S, Jiménez JM, El Yousfi F, Muñoz L (2000) Nitrogen and phosphorus removal from urban wastewater by the microalga Scenedesmus obliquus. Bioresour Technol 73:263–272Google Scholar
  32. Nguyen BT, Rittmann BE (2015) Predicting dissolved inorganic carbon in photoautotrophic microalgae culture via the nitrogen source. Environ Sci Technol 49:9826–9831PubMedGoogle Scholar
  33. Pancha I, Chokshi K, George B, Ghosh T, Paliwal C, Maurya R, Mishra S (2014) Nitrogen stress triggered biochemical and morphological changes in the microalgae Scenedesmus sp. Bioresour Technol 156:146–154PubMedGoogle Scholar
  34. Pegallapati AK, Nirmalakhandan N (2013) Internally illuminated photobioreactor for algal cultivation under carbon dioxide-supplementation: performance evaluation. Renew Energy 56:129–135Google Scholar
  35. Piltz B, Melkonian M (2018) Immobilized microalgae for nutrient recovery from source-separated human urine. J Appl Phycol 30:421–429Google Scholar
  36. Raven JA, Wollenweber B, Handley L (1992) A comparison of ammonium and nitrate as nitrogen sources for photolithotrophs. New Phytol 121:19–32Google Scholar
  37. Rugnini L, Costa G, Congestri R, Antonaroli S, Sanità di Toppi L, Bruno L (2018) Phosphorus and metal removal combined with lipid production by the green microalga Desmodesmus sp.: an integrated approach. Plant Physiol Biochem 125:45–51PubMedGoogle Scholar
  38. Ryu HJ, Oh KK, Kim YS (2009) Optimization of the influential factors for the improvement of CO2 utilization efficiency and CO2 mass transfer rate. J Ind Eng Chem 15:471–475Google Scholar
  39. Sakshaug E, Bricaud A, Dandonneau Y, Falkowski PG, Kiefer DA, Legendre L, Morel A, Parslow J, Takahashi M (1997) Parameters of photosynthesis: definitions, theory and interpretation of results. J Plankton Res 19:1637–1670Google Scholar
  40. Samorì G, Samorì C, Guerrini F, Pistocchi R (2013) Growth and nitrogen removal capacity of Desmodesmus communis and of a natural microalgae consortium in a batch culture system in view of urban wastewater treatment: part I. Water Res 47:791–801PubMedGoogle Scholar
  41. Samorì G, Samorì C, Pistocchi R (2014) Nutrient removal efficiency and physiological responses of Desmodesmus communis at different HRTs and nutrient stress condition using different sources of urban wastewater effluents. Appl Biochem Biotechnol 173:74–89PubMedGoogle Scholar
  42. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96PubMedGoogle Scholar
  43. Sriram S, Seenivasan R (2015) Biophotonic perception on Desmodesmus sp. VIT growth, lipid and carbohydrate content. Bioresour Technol 198:626–633PubMedGoogle Scholar
  44. Uggetti E, Sialve B, Latrille E, Steyer JP (2014) Anaerobic digestate as substrate for microalgae culture: the role of ammonium concentration on the microalgae productivity. Bioresour Technol 152:437–443PubMedGoogle Scholar
  45. Ullrich WR (1983) Uptake and reduction of nitrate: algae and fungi. In: Lauchli A, Bieleski RL (eds) Encyclopedia of Plant Physiology, vol 15 A. Springer-Verlag, Berlin, pp 376–406Google Scholar
  46. Wu LF, Chen PC, Lee CM (2013) The effects of nitrogen sources and temperature on cell growth and lipid accumulation of microalgae. Int Biodeterior Biodegrad 85:506–510Google Scholar
  47. Xin L, Hong-ying H, Ke G, Jia Y (2010a) Growth and nutrient removal properties of a freshwater microalga Scenedesmus sp. LX1 under different kinds of nitrogen sources. Ecol Eng 36:379–381Google Scholar
  48. Xin L, Hong-ying H, Ke G, Ying-xue S (2010b) Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresour Technol 101:5494–5500PubMedGoogle Scholar
  49. Zhuang LL, Azimi Y, Yu D, Wu YH, Hu HY (2018) Effects of nitrogen and phosphorus concentrations on the growth of microalgae Scenedesmus. LX1 in suspended-solid phase photobioreactors (ssPBR). Biomass Bioenergy 109:47–53Google Scholar
  50. Zhuang LL, Wu YH, Espinosa VMD, Zhang TY, Dao GH, Hu HY (2016) Soluble algal products (SAPs) in large scale cultivation of microalgae for biomass/bioenergy production: a review. Renew Sust Energ Rev 59:141–148Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Biological, Geological and Environmental Sciences (BiGeA)University of BolognaRavennaItaly
  2. 2.Department of Chemical, Biological, Pharmaceutical and Environmental Sciences (ChiBioFarAm)University of MessinaMessinaItaly

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