Research Article
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Combined effect of nitrogen and phosphorus on growth and biochemical composition of Tetradesmus obliquus (Turpin) M.J. Wynne

Year 2022, Volume: 9 Issue: 4, 525 - 537, 21.12.2022
https://doi.org/10.21448/ijsm.1102592

Abstract

Microalgae have many biotechnological applications in various industries including food and feed, fertilizer, biofuel, cosmetics, pharmaceutics, and wastewater treatment. Since hey produce secondary metabolites under stress conditions such as pigments, carotenoids, hydrocarbons, and vitamins, investigating the effects of stress factors on growth parameters and biochemical composition of microalgal biomass is needed in producing bioproducts.
In this paper, the combined effects of nitrogen and phosphorus on growth and the protein/amino acid and Lipid-FAMEs profiles of microalgae Tetradesmus obliquus (MAKUMACC-037) were investigated.
Nitrogen and phosphorus deficiency reduced the algal growth. Biochemical composition was changed in a nitrogen and phosphorus dependent manner.
High concentration of protein and lipid were associated with increased nitrogen and phosphorus concentration However, the FAMEs profiles were changed depending on only the nitrogen concentration.

Supporting Institution

Burdur MEhmet AKif Ersoy Universitesi

Project Number

0455-MP-17

References

  • Amaro. H.M., Guedes. A.C., & Malcata. F.X. (2011). Advances and perspectives in using microalgae to produce biodiesel. Applied Energy. 88(10). 3402 3410. https://doi.org/10.1016/J.APENERGY.2010.12.014
  • Anand. J., & Arumugam. M. (2015). Enhanced lipid accumulation and biomass yield of Scenedesmus quadricauda under nitrogen starved condition. Bioresource Technology. 188. 190–194. https://doi.org/10.1016/J.BIORTECH.2014.12.097
  • Atiku. H., Mohamed. R., Al-Gheethi. A., Wurochekke. A., & Kassim. A.H.M. (2016). Harvesting of microalgae biomass from the phytoremediation process of greywater. Environmental Science and Pollution Research. 23(24). 24624 24641. https://doi.org/10.1007/S11356-016-7456-9
  • Beuckels. A., Smolders. E., & Muylaert. K. (2015). Nitrogen availability influences phosphorus removal in microalgae-based wastewater treatment. Water Research. 77. 98–106. https://doi.org/10.1016/J.WATRES.2015.03.018
  • Bongiovani. N., Popovich. C.A., Martínez. A.M., Constenla. D., & Leonardi. P.I. (2020). Biorefinery Approach from Nannochloropsis oceanica CCALA 978: Neutral Lipid and Carotenoid Co-Production Under Nitrate or Phosphate Deprivation. Bioenergy Research. 13(2). 518–529. https://doi.org/10.1007/S12155-019-10045-2/TABLES/2
  • Boussiba. S., Fan. L., & Vonshak. A. (1992). Enhancement and determination of astaxanthin accumulation in green alga Haematococcus pluvialis. Methods in Enzymology. 213(C). 386–391. https://doi.org/10.1016/0076-6879(92)13140-S
  • Breuer. G., Lamers. P.P., Martens. D.E., Draaisma. R.B., & Wijffels. R.H. (2012). The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresource Technology. 124. 217 226. https://doi.org/10.1016/J.BIORTECH.2012.08.003
  • Bligh. E. G., & Dyer. W.J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology. 37(8). 911-917.
  • Cao. J., Yuan. H.L., Li. B.Z., & Yang. J.S. (2014). Significance evaluation of the effects of environmental factors on the lipid accumulation of Chlorella minutissima UTEX 2341 under low-nutrition heterotrophic condition. Bioresource Technology. 152. 177–184. https://doi.org/10.1016/J.BIORTECH.2013.10.084
  • Chia. M.A., Lombardi. A.T., & Melão. M. da G.G. (2013). Growth and biochemical composition of Chlorella vulgaris in different growth media. Anais Da Academia Brasileira de Ciencias. 85(4). 1427–1438. https://doi.org/10.1590/0001-3765201393312
  • Chu. F.F., Chu. P.N., Shen. X.F., Lam. P.K.S., & Zeng. R.J. (2014). Effect of phosphorus on biodiesel production from Scenedesmus obliquus under nitrogen-deficiency stress. Bioresource Technology. 152. 241–246. https://doi.org/10.1016/J.BIORTECH.2013.11.013
  • Cointet. E., Wielgosz-Collin. G., Bougaran. G., Rabesaotra. V., Gonçalves. O., & Méléder. V. (2019). Effects of light and nitrogen availability on photosynthetic efficiency and fatty acid content of three original benthic diatom strains. Plos One. 14(11). e0224701. https://doi.org/10.1371/JOURNAL.PONE.0224701
  • Courchesne. N.M.D., Parisien. A., Wang. B., & Lan. C.Q. (2009). Enhancement of lipid production using biochemical. genetic and transcription factor engineering approaches. Journal of Biotechnology. 141(12). 31 41. https://doi.org/10.1016/J.JBIOTEC.2009.02.018
  • FAO. 2017. The future of food and agriculture – Trends and challenges. Rome.
  • Fernandes. B., Teixeira. J., Dragone. G., Vicente. A. A., Kawano. S., Bišová. K., Přibyl. P., Zachleder. V., & Vítová. M. (2013). Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresource Technology. 144. 268–274. https://doi.org/10.1016/J.BIORTECH.2013.06.096
  • Gao. B., Liu. J., Zhang. C., & Van de Waal. D.B. (2018). Biological stoichiometry of oleaginous microalgal lipid synthesis: The role of N:P supply ratios and growth rate on microalgal elemental and biochemical composition. Algal Research. 32. 353 361. https://doi.org/10.1016/J.ALGAL.2018.04.019
  • Gao. Y., Yang. M., & Wang. C. (2013). Nutrient deprivation enhances lipid content in marine microalgae. Bioresource Technology. 147. 484 491. https://doi.org/10.1016/J.BIORTECH.2013.08.066
  • Godoy-Hernández. G., & Vázquez-Flota. F.A. (2006). Growth Measurements. Methods in Molecular Biology. 318. 51–58. https://doi.org/10.1385/1-59259-959-1:051
  • Hempel. N., Petrick. I., & Behrendt. F. (2012). Biomass productivity and productivity of fatty acids and amino acids of microalgae strains as key characteristics of suitability for biodiesel production. Journal of Applied Phycology. 24(6). 1407 1418. https://doi.org/10.1007/s10811-012-9795-3
  • Ho. S.H., Chan. M.C., Liu. C.C., Chen. C.Y., Lee. W.L., Lee. D.J., & Chang. J.S. (2014). Enhancing lutein productivity of an indigenous microalga Scenedesmus obliquus FSP-3 using light-related strategies. Bioresource Technology. 152. 275–282. https://doi.org/10.1016/J.BIORTECH.2013.11.031
  • Hockin. N.L., Mock. T., Mulholland. F., Kopriva. S., & Malin. G. (2012). The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiology. 158(1). 299–312. https://doi.org/10.1104/PP.111.184333
  • Huang. Y., Lou. C., Luo. L., & Wang. X.C. (2021). Insight into nitrogen and phosphorus coupling effects on mixotrophic Chlorella vulgaris growth under stably controlled nutrient conditions. Science of the Total Environment. 752. 141747. https://doi.org/10.1016/j.scitotenv.2020.141747
  • Imamura. S., Terashita. M., Ohnuma. M., Maruyama. S., Minoda. A., Weber. A.P.M., Inouye. T., Sekine. Y., Fujita. Y., Omata. T., & Tanaka. K. (2010). Nitrate assimilatory genes and their transcriptional regulation in a unicellular red alga cyanidioschyzon merolae: genetic evidence for nitrite reduction by a sulfite reductase-like enzyme. Plant and Cell Physiology. 51(5). 707–717. https://doi.org/10.1093/PCP/PCQ043
  • Ji. C.F., Yu. X.J., Chen. Z.A., Xue. S., Legrand. J., & Zhang. W. (2011). Effects of nutrient deprivation on biochemical compositions and photo-hydrogen production of Tetraselmis subcordiformis. International Journal of Hydrogen Energy. 36(10). 5817–5821. https://doi.org/10.1016/J.IJHYDENE.2010.12.138
  • Ji. F., Hao. R., Liu. Y., Li. G., Zhou. Y., & Dong. R. (2013). Isolation of a novel microalgae strain Desmodesmus sp. and optimization of environmental factors for its biomass production. Bioresource Technology. 148. 249–254. https://doi.org/10.1016/J.BIORTECH.2013.08.110
  • Köse. S., Kaklikkaya. N., Koral. S., Tufan. B., Buruk. K.C., & Aydin. F. (2011). Commercial test kits and the determination of histamine in traditional (ethnic) fish products-evaluation against an EU accepted HPLC method. Food Chemistry. 125(4). 1490–1497. https://doi.org/10.1016/J.FOODCHEM.2010.10.069
  • Li. K., Liu. Q., Fang. F., Luo. R., Lu. Q., Zhou. W., Huo. S., Cheng. P., Liu. J., Addy. M., Chen. P., Chen. D., & Ruan. R. (2019). Microalgae-based wastewater treatment for nutrients recovery: A review. Bioresource Technology. 291. 121934. https://doi.org/10.1016/J.BIORTECH.2019.121934
  • Lin. H., Shavezipur. M., Yousef. A., & Maleky. F. (2016). Prediction of growth of Pseudomonas fluorescens in milk during storage under fluctuating temperature. Journal of Dairy Science. 99(3). 1822–1830. https://doi.org/10.3168/JDS.2015-10179
  • López. C.V.G., del Carmen Cerón García. M., Fernández. F.G.A., Bustos. C.S., Chisti. Y., & Sevilla. J. M. F. (2010). Protein measurements of microalgal and cyanobacterial biomass. Bioresource Technology. 101(19). 7587-7591 .https://doi.org/10.1016/J.BIORTECH.2010.04.077
  • Maizatul. A.Y., Radin Mohamed. R.M.S., Al-Gheethi. A.A., & Hashim. M.K.A. (2017). An overview of the utilisation of microalgae biomass derived from nutrient recycling of wet market wastewater and slaughterhouse wastewater. International Aquatic Research. 9(3). 177–193. https://doi.org/10.1007/S40071-017-0168-Z/TABLES/8
  • Merzlyak. M.N., Chivkunova. O.B., Gorelova. O.A., Reshetnikova. I.V., Solovchenko. A.E., Khozin-Goldberg. I., & Cohen. Z. (2007). Effect of nitrogen starvation on optical propertıes. pigments. and arachidonic acid content of the unicellular green alga Parietochlorıs incisa (trebouxiophyceae. Chlorophyta)1. Journal of Phycology. 43(4). 833–843. https://doi.org/10.1111/J.1529-8817.2007.00375.X
  • Metcalfe. L.D., Schmitz. A.A., & Pelka. J.R. (1966). Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Analytical chemistry. 38(3). 514-515
  • Přibyl. P., Cepák. V., & Zachleder. V. (2014). Oil Overproduction by Means of Microalgae. Algal Biorefineries. 1. 241–273. https://doi.org/10.1007/978-94-007-7494-0_10
  • Procházková. G., Brányiková. I., Zachleder. V., & Brányik. T. (2014). Effect of nutrient supply status on biomass composition of eukaryotic green microalgae. Journal of Applied Phycology. 26(3). 1359–1377. https://doi.org/10.1007/S10811-013-0154-9/TABLES/2
  • Radakovits. R., Jinkerson. R.E., Darzins. A., & Posewitz. M.C. (2010). Genetic engineering of algae for enhanced biofuel production. Eukaryotic Cell. 9(4). 486–501. https://doi.org/10.1128/EC.00364-09/ASSET/CFE6817C-EED9-4151-8ABD-4A098B6BE4CF/ASSETS/GRAPHIC/ZEK9990935090003.JPEG
  • Rani. S., Chowdhury. R., Tao. W., & Srinivasan. A. (2020). Tertiary treatment of municipal wastewater using isolated algal strains: treatment efficiency and value-added products recovery. Chemistry and Ecology. 36(1). 48 65. https://doi.org/10.1080/02757540.2019.1688307/SUPPL_FILE/GCHE_A_1688307_SM0210.DOCX
  • Rippka. R., Deruelles. J., Waterbury. J.B., Herdman. M., & Stanier. R.Y. (1979). Generic Assignments. Strain Histories and Properties of Pure Cultures of Cyanobacteria. Microbiology. 111(1). 1–61. https://doi.org/10.1099/00221287-111-1-1
  • Ross. M.E., Davis. K., McColl. R., Stanley. M.S., Day. J.G., & Semião. A.J.C. (2018). Nitrogen uptake by the macro-algae Cladophora coelothrix and Cladophora parriaudii: Influence on growth. nitrogen preference and biochemical composition. Algal Research. 30. 1–10. https://doi.org/10.1016/J.ALGAL.2017.12.005
  • Salbitani. G., & Carfagna. S. (2020). Different Behaviour between Autotrophic and Heterotrophic Galdieria sulphuraria (Rhodophyta) Cells to Nitrogen Starvation and Restoration. Impact on Pigment and Free Amino Acid Contents. International Journal of Plant Biology. 7. 11(1). 8567. https://doi.org/10.4081/PB.2020.8567
  • Santos-Ballardo. D.U., Rossi. S., Hernández. V., Gómez. R.V., del Carmen Rendón-Unceta. M., Caro-Corrales. J., & Valdez-Ortiz. A. (2015). A simple spectrophotometric method for biomass measurement of important microalgae species in aquaculture. Aquaculture. 448. 87–92. https://doi.org/10.1016/J.AQUACULTURE.2015.05.044
  • Singh. P., Guldhe. A., Kumari. S., Rawat. I., & Bux. F. (2015). Investigation of combined effect of nitrogen. phosphorus and iron on lipid productivity of microalgae Ankistrodesmus falcatus KJ671624 using response surface methodology. Biochemical Engineering Journal. 94. 22–29. https://doi.org/10.1016/J.BEJ.2014.10.019
  • Sirakov. I., Velichkova. K., Stoyanova. S., & Staykov. Y. (2015). The importance of microalgae for aquaculture industry. Rewiev. International Journal of Fisheries and Aquatic Studies. 2(4). 31-37.
  • Tarazona Delgado. R., Guarieiro. M. dos S., Antunes. P.W., Cassini. S.T., Terreros. H.M., & Fernandes. V. de O. (2021). Effect of nitrogen limitation on growth. biochemical composition. and cell ultrastructure of the microalga Picocystis salinarum. Journal of Applied Phycology. 33(4). 2083–2092. https://doi.org/10.1007/S10811-021-02462-8
  • Van Vooren. G., Le Grand. F., Legrand. J., Cuiné. S., Peltier. G., & Pruvost. J. (2012). Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Bioresource Technology. 124. 421–432. https://doi.org/10.1016/J.BIORTECH.2012.08.009
  • Vona. V., Di Martino Rigano. V., Esposito. S., Carillo. P., Carfagna. S., & Rigano. C. (1999). Growth. photosynthesis. and respiration of Chlorella sorokiniana after N-starvation. Interactions between light. CO2 and NH4+ supply. Physiologia Plantarum. 105(2). 288–293. https://doi.org/10.1034/J.1399-3054.1999.105214.X
  • Wynne. M.J., & Hallan. J.K. (2015). Reinstatement of Tetradesmus G.M. Smith (Sphaeropleales. Chlorophyta). Feddes Repertorium. 126(3 4). 83 86. https://doi.org/10.1002/FEDR.201500021
  • Xin. L., Hong-ying. H., Ke. G., & Ying-xue. S. (2010). Effects of different nitrogen and phosphorus concentrations on the growth. nutrient uptake. and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresource Technology. 101(14). 5494–5500. https://doi.org/10.1016/J.BIORTECH.2010.02.016
  • Yaakob. M.A., Mohamed. R.M.S.R., Al-Gheethi. A., Ravishankar. G.A., & Ambati. R.R. (2021). Influence of nitrogen and phosphorus on microalgal growth. biomass. lipid. and fatty acid production: An Overview. Cells. 10(2). 393.https://doi.org/10.3390/CELLS10020393
  • Yodsuwan. N., Sawayama. S., & Sirisansaneeyakul. S. (2017). Effect of nitrogen concentration on growth. lipid production and fatty acid profiles of the marine diatom Phaeodactylum tricornutum. Agriculture and Natural Resources. 51(3). 190–197. https://doi.org/10.1016/J.ANRES.2017.02.004
  • Zarrinmehr. M.J., Farhadian. O., Heyrati. F.P., Keramat. J., Koutra. E., Kornaros. M., & Daneshvar. E. (2020). Effect of nitrogen concentration on the growth rate and biochemical composition of the microalga. Isochrysis galbana. Egyptian Journal of Aquatic Research. 46(2). 153–158. https://doi.org/10.1016/j.ejar.2019.11.003
  • 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. https://doi.org/10.1016/J.BIORTECH.2013.10.092
  • Zhuang. L.L., Azimi. Y., Yu. D., Wu. Y.H., & Hu. H.Y. (2018). Effects of nitrogen and phosphorus concentrations on the growth of microalgae Scenedesmus. LX1 in suspended-solid phase photobioreactors (ssPBR). Biomass and Bioenergy. 109. 47–53. https://doi.org/10.1016/j.biombioe.2017.12.017

Combined effect of nitrogen and phosphorus on growth and biochemical composition of Tetradesmus obliquus (Turpin) M.J. Wynne

Year 2022, Volume: 9 Issue: 4, 525 - 537, 21.12.2022
https://doi.org/10.21448/ijsm.1102592

Abstract

Microalgae have many biotechnological applications in various industries including food and feed, fertilizer, biofuel, cosmetics, pharmaceutics, and wastewater treatment. Since hey produce secondary metabolites under stress conditions such as pigments, carotenoids, hydrocarbons, and vitamins, investigating the effects of stress factors on growth parameters and biochemical composition of microalgal biomass is needed in producing bioproducts.
In this paper, the combined effects of nitrogen and phosphorus on growth and the protein/amino acid and Lipid-FAMEs profiles of microalgae Tetradesmus obliquus (MAKUMACC-037) were investigated.
Nitrogen and phosphorus deficiency reduced the algal growth. Biochemical composition was changed in a nitrogen and phosphorus dependent manner.
High concentration of protein and lipid were associated with increased nitrogen and phosphorus concentration However, the FAMEs profiles were changed depending on only the nitrogen concentration.

Project Number

0455-MP-17

References

  • Amaro. H.M., Guedes. A.C., & Malcata. F.X. (2011). Advances and perspectives in using microalgae to produce biodiesel. Applied Energy. 88(10). 3402 3410. https://doi.org/10.1016/J.APENERGY.2010.12.014
  • Anand. J., & Arumugam. M. (2015). Enhanced lipid accumulation and biomass yield of Scenedesmus quadricauda under nitrogen starved condition. Bioresource Technology. 188. 190–194. https://doi.org/10.1016/J.BIORTECH.2014.12.097
  • Atiku. H., Mohamed. R., Al-Gheethi. A., Wurochekke. A., & Kassim. A.H.M. (2016). Harvesting of microalgae biomass from the phytoremediation process of greywater. Environmental Science and Pollution Research. 23(24). 24624 24641. https://doi.org/10.1007/S11356-016-7456-9
  • Beuckels. A., Smolders. E., & Muylaert. K. (2015). Nitrogen availability influences phosphorus removal in microalgae-based wastewater treatment. Water Research. 77. 98–106. https://doi.org/10.1016/J.WATRES.2015.03.018
  • Bongiovani. N., Popovich. C.A., Martínez. A.M., Constenla. D., & Leonardi. P.I. (2020). Biorefinery Approach from Nannochloropsis oceanica CCALA 978: Neutral Lipid and Carotenoid Co-Production Under Nitrate or Phosphate Deprivation. Bioenergy Research. 13(2). 518–529. https://doi.org/10.1007/S12155-019-10045-2/TABLES/2
  • Boussiba. S., Fan. L., & Vonshak. A. (1992). Enhancement and determination of astaxanthin accumulation in green alga Haematococcus pluvialis. Methods in Enzymology. 213(C). 386–391. https://doi.org/10.1016/0076-6879(92)13140-S
  • Breuer. G., Lamers. P.P., Martens. D.E., Draaisma. R.B., & Wijffels. R.H. (2012). The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresource Technology. 124. 217 226. https://doi.org/10.1016/J.BIORTECH.2012.08.003
  • Bligh. E. G., & Dyer. W.J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology. 37(8). 911-917.
  • Cao. J., Yuan. H.L., Li. B.Z., & Yang. J.S. (2014). Significance evaluation of the effects of environmental factors on the lipid accumulation of Chlorella minutissima UTEX 2341 under low-nutrition heterotrophic condition. Bioresource Technology. 152. 177–184. https://doi.org/10.1016/J.BIORTECH.2013.10.084
  • Chia. M.A., Lombardi. A.T., & Melão. M. da G.G. (2013). Growth and biochemical composition of Chlorella vulgaris in different growth media. Anais Da Academia Brasileira de Ciencias. 85(4). 1427–1438. https://doi.org/10.1590/0001-3765201393312
  • Chu. F.F., Chu. P.N., Shen. X.F., Lam. P.K.S., & Zeng. R.J. (2014). Effect of phosphorus on biodiesel production from Scenedesmus obliquus under nitrogen-deficiency stress. Bioresource Technology. 152. 241–246. https://doi.org/10.1016/J.BIORTECH.2013.11.013
  • Cointet. E., Wielgosz-Collin. G., Bougaran. G., Rabesaotra. V., Gonçalves. O., & Méléder. V. (2019). Effects of light and nitrogen availability on photosynthetic efficiency and fatty acid content of three original benthic diatom strains. Plos One. 14(11). e0224701. https://doi.org/10.1371/JOURNAL.PONE.0224701
  • Courchesne. N.M.D., Parisien. A., Wang. B., & Lan. C.Q. (2009). Enhancement of lipid production using biochemical. genetic and transcription factor engineering approaches. Journal of Biotechnology. 141(12). 31 41. https://doi.org/10.1016/J.JBIOTEC.2009.02.018
  • FAO. 2017. The future of food and agriculture – Trends and challenges. Rome.
  • Fernandes. B., Teixeira. J., Dragone. G., Vicente. A. A., Kawano. S., Bišová. K., Přibyl. P., Zachleder. V., & Vítová. M. (2013). Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresource Technology. 144. 268–274. https://doi.org/10.1016/J.BIORTECH.2013.06.096
  • Gao. B., Liu. J., Zhang. C., & Van de Waal. D.B. (2018). Biological stoichiometry of oleaginous microalgal lipid synthesis: The role of N:P supply ratios and growth rate on microalgal elemental and biochemical composition. Algal Research. 32. 353 361. https://doi.org/10.1016/J.ALGAL.2018.04.019
  • Gao. Y., Yang. M., & Wang. C. (2013). Nutrient deprivation enhances lipid content in marine microalgae. Bioresource Technology. 147. 484 491. https://doi.org/10.1016/J.BIORTECH.2013.08.066
  • Godoy-Hernández. G., & Vázquez-Flota. F.A. (2006). Growth Measurements. Methods in Molecular Biology. 318. 51–58. https://doi.org/10.1385/1-59259-959-1:051
  • Hempel. N., Petrick. I., & Behrendt. F. (2012). Biomass productivity and productivity of fatty acids and amino acids of microalgae strains as key characteristics of suitability for biodiesel production. Journal of Applied Phycology. 24(6). 1407 1418. https://doi.org/10.1007/s10811-012-9795-3
  • Ho. S.H., Chan. M.C., Liu. C.C., Chen. C.Y., Lee. W.L., Lee. D.J., & Chang. J.S. (2014). Enhancing lutein productivity of an indigenous microalga Scenedesmus obliquus FSP-3 using light-related strategies. Bioresource Technology. 152. 275–282. https://doi.org/10.1016/J.BIORTECH.2013.11.031
  • Hockin. N.L., Mock. T., Mulholland. F., Kopriva. S., & Malin. G. (2012). The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiology. 158(1). 299–312. https://doi.org/10.1104/PP.111.184333
  • Huang. Y., Lou. C., Luo. L., & Wang. X.C. (2021). Insight into nitrogen and phosphorus coupling effects on mixotrophic Chlorella vulgaris growth under stably controlled nutrient conditions. Science of the Total Environment. 752. 141747. https://doi.org/10.1016/j.scitotenv.2020.141747
  • Imamura. S., Terashita. M., Ohnuma. M., Maruyama. S., Minoda. A., Weber. A.P.M., Inouye. T., Sekine. Y., Fujita. Y., Omata. T., & Tanaka. K. (2010). Nitrate assimilatory genes and their transcriptional regulation in a unicellular red alga cyanidioschyzon merolae: genetic evidence for nitrite reduction by a sulfite reductase-like enzyme. Plant and Cell Physiology. 51(5). 707–717. https://doi.org/10.1093/PCP/PCQ043
  • Ji. C.F., Yu. X.J., Chen. Z.A., Xue. S., Legrand. J., & Zhang. W. (2011). Effects of nutrient deprivation on biochemical compositions and photo-hydrogen production of Tetraselmis subcordiformis. International Journal of Hydrogen Energy. 36(10). 5817–5821. https://doi.org/10.1016/J.IJHYDENE.2010.12.138
  • Ji. F., Hao. R., Liu. Y., Li. G., Zhou. Y., & Dong. R. (2013). Isolation of a novel microalgae strain Desmodesmus sp. and optimization of environmental factors for its biomass production. Bioresource Technology. 148. 249–254. https://doi.org/10.1016/J.BIORTECH.2013.08.110
  • Köse. S., Kaklikkaya. N., Koral. S., Tufan. B., Buruk. K.C., & Aydin. F. (2011). Commercial test kits and the determination of histamine in traditional (ethnic) fish products-evaluation against an EU accepted HPLC method. Food Chemistry. 125(4). 1490–1497. https://doi.org/10.1016/J.FOODCHEM.2010.10.069
  • Li. K., Liu. Q., Fang. F., Luo. R., Lu. Q., Zhou. W., Huo. S., Cheng. P., Liu. J., Addy. M., Chen. P., Chen. D., & Ruan. R. (2019). Microalgae-based wastewater treatment for nutrients recovery: A review. Bioresource Technology. 291. 121934. https://doi.org/10.1016/J.BIORTECH.2019.121934
  • Lin. H., Shavezipur. M., Yousef. A., & Maleky. F. (2016). Prediction of growth of Pseudomonas fluorescens in milk during storage under fluctuating temperature. Journal of Dairy Science. 99(3). 1822–1830. https://doi.org/10.3168/JDS.2015-10179
  • López. C.V.G., del Carmen Cerón García. M., Fernández. F.G.A., Bustos. C.S., Chisti. Y., & Sevilla. J. M. F. (2010). Protein measurements of microalgal and cyanobacterial biomass. Bioresource Technology. 101(19). 7587-7591 .https://doi.org/10.1016/J.BIORTECH.2010.04.077
  • Maizatul. A.Y., Radin Mohamed. R.M.S., Al-Gheethi. A.A., & Hashim. M.K.A. (2017). An overview of the utilisation of microalgae biomass derived from nutrient recycling of wet market wastewater and slaughterhouse wastewater. International Aquatic Research. 9(3). 177–193. https://doi.org/10.1007/S40071-017-0168-Z/TABLES/8
  • Merzlyak. M.N., Chivkunova. O.B., Gorelova. O.A., Reshetnikova. I.V., Solovchenko. A.E., Khozin-Goldberg. I., & Cohen. Z. (2007). Effect of nitrogen starvation on optical propertıes. pigments. and arachidonic acid content of the unicellular green alga Parietochlorıs incisa (trebouxiophyceae. Chlorophyta)1. Journal of Phycology. 43(4). 833–843. https://doi.org/10.1111/J.1529-8817.2007.00375.X
  • Metcalfe. L.D., Schmitz. A.A., & Pelka. J.R. (1966). Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Analytical chemistry. 38(3). 514-515
  • Přibyl. P., Cepák. V., & Zachleder. V. (2014). Oil Overproduction by Means of Microalgae. Algal Biorefineries. 1. 241–273. https://doi.org/10.1007/978-94-007-7494-0_10
  • Procházková. G., Brányiková. I., Zachleder. V., & Brányik. T. (2014). Effect of nutrient supply status on biomass composition of eukaryotic green microalgae. Journal of Applied Phycology. 26(3). 1359–1377. https://doi.org/10.1007/S10811-013-0154-9/TABLES/2
  • Radakovits. R., Jinkerson. R.E., Darzins. A., & Posewitz. M.C. (2010). Genetic engineering of algae for enhanced biofuel production. Eukaryotic Cell. 9(4). 486–501. https://doi.org/10.1128/EC.00364-09/ASSET/CFE6817C-EED9-4151-8ABD-4A098B6BE4CF/ASSETS/GRAPHIC/ZEK9990935090003.JPEG
  • Rani. S., Chowdhury. R., Tao. W., & Srinivasan. A. (2020). Tertiary treatment of municipal wastewater using isolated algal strains: treatment efficiency and value-added products recovery. Chemistry and Ecology. 36(1). 48 65. https://doi.org/10.1080/02757540.2019.1688307/SUPPL_FILE/GCHE_A_1688307_SM0210.DOCX
  • Rippka. R., Deruelles. J., Waterbury. J.B., Herdman. M., & Stanier. R.Y. (1979). Generic Assignments. Strain Histories and Properties of Pure Cultures of Cyanobacteria. Microbiology. 111(1). 1–61. https://doi.org/10.1099/00221287-111-1-1
  • Ross. M.E., Davis. K., McColl. R., Stanley. M.S., Day. J.G., & Semião. A.J.C. (2018). Nitrogen uptake by the macro-algae Cladophora coelothrix and Cladophora parriaudii: Influence on growth. nitrogen preference and biochemical composition. Algal Research. 30. 1–10. https://doi.org/10.1016/J.ALGAL.2017.12.005
  • Salbitani. G., & Carfagna. S. (2020). Different Behaviour between Autotrophic and Heterotrophic Galdieria sulphuraria (Rhodophyta) Cells to Nitrogen Starvation and Restoration. Impact on Pigment and Free Amino Acid Contents. International Journal of Plant Biology. 7. 11(1). 8567. https://doi.org/10.4081/PB.2020.8567
  • Santos-Ballardo. D.U., Rossi. S., Hernández. V., Gómez. R.V., del Carmen Rendón-Unceta. M., Caro-Corrales. J., & Valdez-Ortiz. A. (2015). A simple spectrophotometric method for biomass measurement of important microalgae species in aquaculture. Aquaculture. 448. 87–92. https://doi.org/10.1016/J.AQUACULTURE.2015.05.044
  • Singh. P., Guldhe. A., Kumari. S., Rawat. I., & Bux. F. (2015). Investigation of combined effect of nitrogen. phosphorus and iron on lipid productivity of microalgae Ankistrodesmus falcatus KJ671624 using response surface methodology. Biochemical Engineering Journal. 94. 22–29. https://doi.org/10.1016/J.BEJ.2014.10.019
  • Sirakov. I., Velichkova. K., Stoyanova. S., & Staykov. Y. (2015). The importance of microalgae for aquaculture industry. Rewiev. International Journal of Fisheries and Aquatic Studies. 2(4). 31-37.
  • Tarazona Delgado. R., Guarieiro. M. dos S., Antunes. P.W., Cassini. S.T., Terreros. H.M., & Fernandes. V. de O. (2021). Effect of nitrogen limitation on growth. biochemical composition. and cell ultrastructure of the microalga Picocystis salinarum. Journal of Applied Phycology. 33(4). 2083–2092. https://doi.org/10.1007/S10811-021-02462-8
  • Van Vooren. G., Le Grand. F., Legrand. J., Cuiné. S., Peltier. G., & Pruvost. J. (2012). Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Bioresource Technology. 124. 421–432. https://doi.org/10.1016/J.BIORTECH.2012.08.009
  • Vona. V., Di Martino Rigano. V., Esposito. S., Carillo. P., Carfagna. S., & Rigano. C. (1999). Growth. photosynthesis. and respiration of Chlorella sorokiniana after N-starvation. Interactions between light. CO2 and NH4+ supply. Physiologia Plantarum. 105(2). 288–293. https://doi.org/10.1034/J.1399-3054.1999.105214.X
  • Wynne. M.J., & Hallan. J.K. (2015). Reinstatement of Tetradesmus G.M. Smith (Sphaeropleales. Chlorophyta). Feddes Repertorium. 126(3 4). 83 86. https://doi.org/10.1002/FEDR.201500021
  • Xin. L., Hong-ying. H., Ke. G., & Ying-xue. S. (2010). Effects of different nitrogen and phosphorus concentrations on the growth. nutrient uptake. and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresource Technology. 101(14). 5494–5500. https://doi.org/10.1016/J.BIORTECH.2010.02.016
  • Yaakob. M.A., Mohamed. R.M.S.R., Al-Gheethi. A., Ravishankar. G.A., & Ambati. R.R. (2021). Influence of nitrogen and phosphorus on microalgal growth. biomass. lipid. and fatty acid production: An Overview. Cells. 10(2). 393.https://doi.org/10.3390/CELLS10020393
  • Yodsuwan. N., Sawayama. S., & Sirisansaneeyakul. S. (2017). Effect of nitrogen concentration on growth. lipid production and fatty acid profiles of the marine diatom Phaeodactylum tricornutum. Agriculture and Natural Resources. 51(3). 190–197. https://doi.org/10.1016/J.ANRES.2017.02.004
  • Zarrinmehr. M.J., Farhadian. O., Heyrati. F.P., Keramat. J., Koutra. E., Kornaros. M., & Daneshvar. E. (2020). Effect of nitrogen concentration on the growth rate and biochemical composition of the microalga. Isochrysis galbana. Egyptian Journal of Aquatic Research. 46(2). 153–158. https://doi.org/10.1016/j.ejar.2019.11.003
  • 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. https://doi.org/10.1016/J.BIORTECH.2013.10.092
  • Zhuang. L.L., Azimi. Y., Yu. D., Wu. Y.H., & Hu. H.Y. (2018). Effects of nitrogen and phosphorus concentrations on the growth of microalgae Scenedesmus. LX1 in suspended-solid phase photobioreactors (ssPBR). Biomass and Bioenergy. 109. 47–53. https://doi.org/10.1016/j.biombioe.2017.12.017
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Details

Primary Language English
Subjects Structural Biology
Journal Section Articles
Authors

Füsun Akgül 0000-0002-2186-5746

Rıza Akgül 0000-0002-0280-2897

Project Number 0455-MP-17
Publication Date December 21, 2022
Submission Date April 13, 2022
Published in Issue Year 2022 Volume: 9 Issue: 4

Cite

APA Akgül, F., & Akgül, R. (2022). Combined effect of nitrogen and phosphorus on growth and biochemical composition of Tetradesmus obliquus (Turpin) M.J. Wynne. International Journal of Secondary Metabolite, 9(4), 525-537. https://doi.org/10.21448/ijsm.1102592
International Journal of Secondary Metabolite

e-ISSN: 2148-6905