Main Article Content

Abstract

In the present manuscript, the growth profile of the microalgae Spirulina sp. NCIM 5143 was studied. Screening was performed on four commercial media, i.e., blue‒green-11 (BG-11), Bold’s basal medium (BBM), algal culture medium (ACM), Zarrouk’s medium (ZM), and different concentrations (20%, 40%, 60%, 80%, and 100%) of unsterilized dairy effluent (UDE). Characterization of biomass was performed to assess its biochemical composition through various assays. Elemental composition and bioactive compound analysis were accomplished by inductively coupled plasma-atomic emission spectroscopy (ICP‒AES) and gas chromatography‒mass spectrometry (GC‒MS), respectively. The results revealed that maximum values of most of the parameters, i.e., optical density (0.21), chlorophyll (2.00 mg/l), proteins (119.17 mg/l), and wet (4.06 g/l) and dry biomass weight (0.28 g/l), were found on ZM. For UDE, maximum growth parameters and the highest nutrient removal efficiency were obtained at 100% concentration. Biochemical analysis revealed that total Kjeldahl nitrogen (7.14±0.49%), crude protein (48.23± 3.34%), total antioxidant activity (3.07±0.03 mg AAE/g), and total phenols (8.88±1.93 mg GAE/g) were present in the biomass. Elemental and GC‒MS analysis detected essential micronutrients and many bioactive compounds, respectively. Hence, this study proved that Spirulina sp. NCIM 5143 has the potential for the management of waste dairy effluent. This study also showed its cost-effectiveness, as the dairy effluent analyzed is used without any kind of sterilization. In addition, its biomass is rich in several essential elements, antioxidants, and bioactive compounds of therapeutic and nutraceutical importance.

Keywords

Antioxidant Dairy Effluent Micronutrient Nutrient removal Phytochemicals Spirulina sp.

Article Details

How to Cite
Sharma, N., & Phutela, U. G. (2023). Analysis of the growth profile, biochemical composition and nutrient removal efficacy of Spirulina sp. NCIM 5143. Environment Conservation Journal, 24(4), 269–286. https://doi.org/10.36953/ECJ.22712574

References

  1. Abd El-Baky, H.H., El Baz, F.K., & El-Baroty, G.S. (2007). Production of carotenoids from marine microalgae and its evaluation as safe food colorant and lowering cholesterol agents. American-Eurasian Journal of Agricultural and Environmental Science, 2(6), 792-800.
  2. Ahamad, F., Sharma, A. K., & Tyagi, S. K. (2023). A Study on Comparative Assessment of Water Quality of Dal and Nigeen Lakes of Jammu and Kashmir, India. Agro Environmental Sustainability, 1(1), 48-56. DOI: https://doi.org/10.59983/s2023010107
  3. Akao, P.K., Singh, B., Kaur, P., Sor, A., Avni, A., Dhir, A., Verma, S., Kapoor, S., Phutela, U.G., Satpute, S., Sharma, S., Avisar, D., Sandha, K.S. & Mamane, H. (2021). Coupled microalgal–bacterial biofilm for enhanced wastewater treatment without energy investment. Journal of Water Process Engineering. Vol. 41:102029 DOI: https://doi.org/10.1016/j.jwpe.2021.102029
  4. Andrade, B.B., Cardoso, L.G., Assis, D.J., Costa, J.A.V., Druzian, J.I., & Lima, S.T.C. (2019). Production and characterization of Spirulina sp. LEB 18 cultured in reused Zarrouk’s medium in a raceway-type bioreactor. Bioresource Technology, 284, 340–348. DOI: https://doi.org/10.1016/j.biortech.2019.03.144
  5. Anvara, A.A., & Nowruzib, B. (2014). Nutritional value of spirulina and its use in the preparation of some complementary baby food formulas. Journal of Agroalimentary Processes and Technologies, 20, 330-350.
  6. AOAC, (1990). Association of official analytical chemists, official methods of analysis. 15th ed. Washington DC.
  7. APHA, (2005). Standard Methods for Examination of Water and Wastewater 21st Edition, American Public Health Association/American Water Works Association/Water Environment Federation, Washington DC, USA.
  8. Ariede, M.B., Candido, T.M., Jacome, A.L.M., Velasco, M.V.R., de Carvalho, J.C.M., & Baby, A.R. (2017). Cosmetic attributes of algae—A review. Algal Research, 25, 483–487, doi:10.1016/j.algal.2017.05.019. DOI: https://doi.org/10.1016/j.algal.2017.05.019
  9. Awuchi, & Godswill, C. (2020). Health Benefits of Micronutrients (Vitamins and Minerals) and their Associated Deficiency Diseases: A Systematic Review. International Journal of Food Sciences, 3,1-32. DOI: https://doi.org/10.47604/ijf.1024
  10. Bajwa, K., Bishnoi, N.R., Kirrolia, A., Sharma, J., & Gupta, S. (2017). Comparison of various growth media composition for physio-biochemical parameters of biodiesel producing microalgal species (Chlorococcum aquaticum, Scenedesmus obliquus, Nannochloropsisoculata, Chlorella pyrenoidosa). European Journal of Biotechnology and Bioscience,5, 27-31.
  11. Banwo, K., Olojede, A.O., Adesulu-Dahunsi, A.T., Verma, D.K., Thakur, M., Tripathy, S., Singh, S., Patel, A.R., Gupta, A.K., Aguilar, C.N., Utama, G.L. (2021) Functional importance of bioactive compounds of foods with Potential Health Benefits: A review on recent trends. Food Bioscience. 43, 1-23. DOI: https://doi.org/10.1016/j.fbio.2021.101320
  12. Beltrán-Rocha, J.C., Guajardo-Barbosa, C., Barceló-Quinta, I.D. & López-Chuken, U.J. (2017). Biotratamiento de efluentes secundarios municipales utilizando microalgas: Efecto del pH, nutrientes (C, N y P) y enriquecimiento con CO2. Revista de Biologia Marina y Oceanografia, 52, 417–427. https://doi.org/10.4067/s0718-19572017000300001 DOI: https://doi.org/10.4067/S0718-19572017000300001
  13. Berdanier, C.D., Dwyer, J.T., Johanna, T., & David, H. (2013). Handbook of Nutrition and Food (3rd ed.). CRC Press. p. 199. ISBN 978-1-4665-0572-8.
  14. Bhutiani, R., Ahamad, F., & Ruhela, M. (2021). Effect of composition and depth of filter-bed on the efficiency of Sand-intermittent-filter treating the Industrial wastewater at Haridwar, India. Journal of Applied and Natural Science, 13(1), 88-94. DOI: https://doi.org/10.31018/jans.v13i1.2421
  15. Bhutiani, R., & Ahamad, F. (2018). Efficiency assessment of Sand Intermittent Filtration Technology for waste water Treatment. International Journal of advance research in science and engineering (IJARSE), 7(03), 503-512.
  16. Bhutiani, R., Ahamad, F., Tyagi, V., & Ram, K. (2018). Evaluation of water quality of River Malin using water quality index (WQI) at Najibabad, Bijnor (UP) India. Environment Conservation Journal, 19(1&2), 191-201. DOI: https://doi.org/10.36953/ECJ.2018.191228
  17. Bojago, E., Tyagi, I., Ahamad, F., & Chandniha, S. K. (2023). GIS based spatial-temporal distribution of water quality parameters and heavy metals in drinking water: Ecological and health modelling. Physics and Chemistry of the Earth, Parts A/B/C, 103399. DOI: https://doi.org/10.1016/j.pce.2023.103399
  18. Braga, V.S., Mastrantonio, D.J.S., Costa, J.A.V., & Morais, M.G. (2018). Cultivation strategy to stimulate high carbohydrate content in Spirulina biomass. Bioresource Technology, 269, 221–226. DOI: https://doi.org/10.1016/j.biortech.2018.08.105
  19. Cardoso, L.G., Duarte, J.H., Costa, J.A.V., Assis, D. de J., Lemos, P.V.F., Druzian, J.I., Souza, C.O.de, Nunes, I.L., & Chinalia, F.A. (2020) Spirulina sp. as a Bioremediation Agent for Aquaculture Wastewater: Production of High Added Value Compounds and Estimation of Theoretical Biodiesel. Bioenergy Research, 14, 254–264 DOI: https://doi.org/10.1007/s12155-020-10153-4
  20. Chandrasekaran, M., Senthilkumar, A., & Venkatesalu, V. (2011). Antibacterial and antifungal efficacy of fatty acid methyl esters from leaves of Sesuvium portulacastrum L. European Review for Medical and Pharmacological Science, 15, 775-80.
  21. Chaudhary, R., & Tripathy, A. (2015). Isolation and Identification of Bioactive Compounds from Irpex Lacteus Wild Fleshy Fungi. Journal of Pharmaceutical Sciences and Research,7, 424-34.
  22. Chikwe, T.N. & Onojake, M.C. (2016) An appraisal of Physicochemical Parameters and some Trace metals at the Disposal Points of Five Industrial Effluents in Trans-Amadi Industrial Area of Port Harcourt, Nigeria. Journal of Applied Science and Environment Management, 20, 31-37 DOI: https://doi.org/10.4314/jasem.v21i1.4
  23. Choi, H. J. (2016) Dairy wastewater treatment using microalgae for potential biodiesel application. Environment Engineering Research, 21, 393-400. DOI: https://doi.org/10.4491/eer.2015.151
  24. Daneshvar, E., Antikainen, L., Koutra, E., Kornaros, M., & Bhatnagar, A. (2018). Investigation on the feasibility of Chlorella vulgaris cultivation in a mixture of pulp and aquaculture effluents: treatment of wastewater and lipid extraction. Bioresource Technology, 255,104–110. https://doi.org/10.1016/j.biortech.2018.01.101. DOI: https://doi.org/10.1016/j.biortech.2018.01.101
  25. Dar, R.A. (2017). Bioprospects of microalgal isolates from water logged area of Punjab for biogas production. Ph.D. thesis, Punjab Agricultural University, Ludhiana, Punjab.
  26. Dar, R.A., & Phutela, U.G. (2020). Enzymatic and hydrothermal pretreatment of newly isolated Spirulina subsalsa BGLR6 biomass for enhanced biogas production. Waste and Biomass Valorization,11, 3639-3651. DOI: https://doi.org/10.1007/s12649-019-00712-y
  27. Demirel, B., Yenigun, O., & Onay, T.T. (2005). Anaerobic treatment of dairy wastewaters: A review. Process Biochemistry, 40, 2583–95. DOI: https://doi.org/10.1016/j.procbio.2004.12.015
  28. Ding, J., Zhao. F., Cao. Y., Xing, L., Liu, W., Mei, S., &Li, S. (2015). Cultivation of microalgae in dairy farm wastewater without sterilization. International Journal of Phytoremediation,17, 222-27. DOI: https://doi.org/10.1080/15226514.2013.876970
  29. DuBois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–56. DOI: https://doi.org/10.1021/ac60111a017
  30. El-Baky, H.H.A., El-Baz, F.K., & El-Baroty, G.S. (2008). Characterization of nutraceutical compounds in blue green alga Spirulina maxima. Journal of Medicinal Plants Research, 2, 292-300.
  31. Falkowski, P.G. (1984). Physiological responses of phytoplankton to natural light regimes. Journal of Plankton Research, 6, 295-307. DOI: https://doi.org/10.1093/plankt/6.2.295
  32. Gernand, A.D., Schulze, K.J., Stewart, C.P., West, Jr. K.P., & Christian, P. (2016). Micronutrient deficiencies in pregnancy worldwide: Health effects and prevention. Nature Reviews Endocrinology, 12, 274–289. DOI: https://doi.org/10.1038/nrendo.2016.37
  33. Girard, J.M., Roy, M.L., Hafsa, M.B., Gagnon, J., Faucheux, N., Heitz, M., Tremblay, R., & Deschênes, J-S (2014). Mixotrophic cultivation of green microalgae Scenedesmus obliquus on cheese whey permeate for biodiesel production. Algae Research, 5, 241–248. DOI: https://doi.org/10.1016/j.algal.2014.03.002
  34. Hendricks, I. & David, W. (2007). Water Treatment Unit Processes: Physical and Chemical. Boca Raton, FL: CRC Press, pp 44–62.
  35. Hseu, Z. (2004). Evaluating heavy metal contents in nine composts using four digestion methods. Bioresource Technology, 95, 53-59. DOI: https://doi.org/10.1016/j.biortech.2004.02.008
  36. Hu, B., Min, M., Zhou, W., Li, Y., Mohr, M., Cheng, Y., Lei, H., Liu, Y., Lin, X., Chen, P., &Ruan, R. (2012). Influence of exogenous CO2 on biomass and lipid accumulation of microalgae Auxenochlorella protothecoides cultivated in concentrated municipal wastewater. Applied Biochemistry and Biotechnology, 166, 1661–73. DOI: https://doi.org/10.1007/s12010-012-9566-2
  37. Jackson, M. L. (1967). Soil Chemical Analysis. Prentice -Hall, Inc., Englewood Cliffs, USA.
  38. Joseph, K. (1995). Pollution control in dairy industry, paper presented at Tamil Nadu veterinary and animal sciences university at veterinary college on 10th Oct 1995, sponsored by the institute of food and dairy technology and Tamil Nadu pollution control board.
  39. Jubie, S., & Dhanaba, S.P. (2012). Gas Chromatography- Mass Spectrometry Analysis and Antibacterial Activity of Fatty acid Mixture of Spirulina platensis. Journal of Pharmaceutical Science and Research, 4, 1836 - 1838
  40. Kameshwari, V., Selvaraj, S., & Sundaramoorthy, S. (2020). Single Cell Protein Spirulina-A Nutrient Treasure. Research Journal of Pharmacology and Pharmacodynamics, 12(2), 49. DOI: https://doi.org/10.5958/2321-5836.2020.00010.5
  41. Kodihalli, M.H., Sriappareddy, T., Haniyambadi, B.M.K., & Yelagiri, M.P. (2018). Screening of potential microalgal species from different natural environment for biodiesel production. International Journal of Microbiology Research, 10, 1052-57. DOI: https://doi.org/10.9735/0975-5276.10.3.1052-1057
  42. Kothari, R., Pathak, V.V., Kumar, V., & Singh, D.P. (2012). Experimental study for growth potential of unicellular alga Chlorella pyrenoidosa on dairy wastewater: An integrated approach for treatment and biofuel production. Bioresource Technology,116, 466–70. DOI: https://doi.org/10.1016/j.biortech.2012.03.121
  43. Kothari, R., Prasad, R., Kumar, V., & Singh, D.P. (2013). Production of biodiesel from microalgae Chlamydomonas polypyrenoideum grown on dairy industry wastewater. Bioresource Technology,144, 499-503. DOI: https://doi.org/10.1016/j.biortech.2013.06.116
  44. Kotteswari, M., Murugesan, S., & Kumar, R. (2012). Phycoremediation of Dairy Effluent by using the Microalgae Nostoc sp. International Journal of Environmental Research and Development, 2, 35-43.
  45. Krishnakumar, S., Bai, V.D.M., & Rajan, R.A. (2013). Evaluation of bioactive metabolites from halophilic microalgae Dunaliella salina by GC‒MS analysis. International Journal of Pharmacy and Pharmaceutical Sciences, 5, 296-303.
  46. Krishnamoorthy, K., & Subramaniam, P. (2014) Phytochemical profiling of leaf, stem, and tuber parts of Solena amplexicaulis (Lam.) Gandhi Using GC‒MS. International Scholarly Research Notices, 2014,1-13 DOI: https://doi.org/10.1155/2014/567409
  47. Kumar, K., Dasgupta, C.N., & Das, D. (2014). Cell growth kinetics of Chlorella sorokiniana and nutritional values of its biomass. Bioresource Technology, 167, 358–366. https://doi.org/10.1016/j.biortech.2014.05.118 DOI: https://doi.org/10.1016/j.biortech.2014.05.118
  48. Kushwaha, J.P., Srivastava, V.C., & Mall, I.D. (2011). An overview of various technologies for the treatment of dairy wastewaters. Critical Reviews in Food Science and Nutrition, 51, 442–52. DOI: https://doi.org/10.1080/10408391003663879
  49. Li, X., Xu, H., & Wu, Q. (2007). Large-scale biodiesel production from microalga Chlorella protothecoides through heterotrophic cultivation in bioreactors. Biotechnology and Bioengineering, 98, 764-71. DOI: https://doi.org/10.1002/bit.21489
  50. Liang, K., Zhang, Q., Gu, M. & Cong, W. (2013). Effect of phosphorus on lipid accumulation in freshwater microalgae Chlorella sp. Journal of Applied Phycology, 25, 311-18. DOI: https://doi.org/10.1007/s10811-012-9865-6
  51. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350-82. DOI: https://doi.org/10.1016/0076-6879(87)48036-1
  52. Liestianty, D., Rodianawati, I., Arfah, R.A., Assa, A., Patimah, Sundari, &Muliadi. (2019). Nutritional analysis of Spirulina sp. to promote as superfood candidate. IOP Conf. Series: Materials Science and Engineering, 509,1-6. DOI: https://doi.org/10.1088/1757-899X/509/1/012031
  53. Loneragan, J.F. & Webb M.J. (1993). Interactions between zinc and other nutrients affecting the growth of plants, Zinc Soils Plants, Springer Netherlands, Dordrecht, pp. 119–134. DOI: https://doi.org/10.1007/978-94-011-0878-2_9
  54. Lowry, O.H., Rosebrough, N.J., Farr, A.L., & Randall, R.J. (1951). Protein measurement with folin-phenol reagent. Journal of Biological Chemistry,193, 265-75. DOI: https://doi.org/10.1016/S0021-9258(19)52451-6
  55. Madkour, F.F., Kamil, A.E., & Nasr, H.S. (2012). Production and nutritive value of Spirulina latensis in reduced cost media. Egyptian Journal of Aquatic Research, 38, 51-7. DOI: https://doi.org/10.1016/j.ejar.2012.09.003
  56. Maehre, H.K., Dalheim, L., Edvinsen, G.K., Elvevoll, E.O., & Jensen, I-J. (2018) Protein Determination-Method Matters. Foods,7, 1-11 DOI: https://doi.org/10.3390/foods7010005
  57. Malaviya, P. & Rathore, V.S. (2001). A correlation study on some physicochemical quality parameters of pulp and paper mill effluents. Pollution Research, 20, 465-70.
  58. Mane, R.S., & Chakraborty, B. (2018). Phytochemical screening of Spirulina platensis extracts from Rankala Lake Kolhapur, India. Journal of Algal Biomass Utilization, 9, 38-41.
  59. Mishra, S.K., Suh, W.I., Farooq, W., Moon, M., Shrivastav, A., Park-Min, S., & Yang, J.W. (2014). Rapid quantification of microalgal lipids in aqueous medium by a simple colorimetric method. Bioresource Technology, 155, 330-33. DOI: https://doi.org/10.1016/j.biortech.2013.12.077
  60. Moghazy, R.M. (2019). Activated biomass of the green microalga Chlamydomonas variabilis as an efficient biosorbent to remove methylene blue dye from aqueous solutions.Water SA, 45, 20-28. DOI: https://doi.org/10.4314/wsa.v45i1.03
  61. Mohan, S.V., Rohit, M.V., Chiranjeevi, P., Chandra, R., & Navaneeth, B. (2015). Heterotrophic microalgae cultivation to synergize biodiesel production with waste remediation: Progress and perspectives. Bioresource Technology, 184, 169–178. DOI: https://doi.org/10.1016/j.biortech.2014.10.056
  62. Musa D, Mu’azu A, Ujih U, Sabiu N, Abubakar M and Gebbe H (2016) Bioconcentration of Heavy Metals by Wild Plants Along Holomorphic Soils in Sule-Tankarkar Local Government Area, Jigawa State, Nigeria. Journal of Natural Sciences Research. 6:18-24.
  63. Olofsson, P., Hultqvist, M., & Holmdahl, M. (2011). Phytol as a cholesterol lowering agent, Pub No.US2011/0015278A1.
  64. Pandey, J.P., Tiwari, A., & Mishra, R.M. (2010). Evaluation of Biomass Production of Spirulina maxima on Different Reported Media. Journal of Algal Biomass Utilization, 1, 70 – 81.
  65. Porwal, H.J., Mane, A.V., & Vehlhal, S.G. (2015). Biodegradation of dairy effluent by using microbial isolates obtained from activated sludge. Water resource and industry,9,1-15. DOI: https://doi.org/10.1016/j.wri.2014.11.002
  66. Prieto, P., Pineda, M., & Aguilar, M. (1999). Spectrophotometric Quantitation of Antioxidant Capacity through the Formation of a Phosphomolybdenum Complex: Specific Application to the Determination of Vitamin E. Analytical Biochemistry,269, 337-41. DOI: https://doi.org/10.1006/abio.1999.4019
  67. Rajasekaran, C., Ajeesh, C.P.M., Balaji, S., Shalini, M., Siva, R., Das, R., Fulzele, D.P., & Kalaivani, T. (2016). Effect of Modified Zarrouk’s Medium on Growth of Different Spirulina Strains. Agriculture Technology and Biological Sciences,13, 67-75.
  68. Ramsundar, P., Abhishek, G., Singh, P., Pillay, K., & Bux, F. (2017). Evaluation of water activated sludge as a potential nutrient source for cultivation of Chlorella sorokiniana. Microalgae Research, 28, 108– 117. DOI: https://doi.org/10.1016/j.algal.2017.10.006
  69. Rao, P.H., Ranjith, K.R., Raghavan, B.G., Subramanian, V.V., & Sivasubramanian, V. (2011). Application of phycoremediation technology in the treatment of wastewater from a leatherprocessing chemical manufacturing facility. Water, 37, N7-14. DOI: https://doi.org/10.4314/wsa.v37i1.64099
  70. Rebolloso-Fuentes, M. M., Navarro-Pérez, A., García-Camacho, F., Ramos-Miras, J. J., & Guil-Guerrero, J.L. (2001). Biomass Nutrient Profiles of the Microalga Nannochloropsis. Journal of Agricultural and Food Chemistry, 49, 2966–2972. DOI: https://doi.org/10.1021/jf0010376
  71. Rechner, A.R., Spencer, J.P.E., Kuhnle, G., Hahn, U., & Rice-Evans, C.A. (2001). Novel biomarkers of the metabolism of caffeic acid derivatives in vivo. Free Radical Biology and Medicine, 30, 1213-1222. DOI: https://doi.org/10.1016/S0891-5849(01)00506-8
  72. Sahana, S.P., & Shirnalli, G.G. (2018). Effect of Microalgae on Physico-Chemical Properties of Different Dilutions of Untreated and Treated Dairy Industrial Effluent International Journal of Current Microbiology and Applied Sciences,7, 2979-93. DOI: https://doi.org/10.20546/ijcmas.2018.704.338
  73. Salama, E., Jeon, B.H., Chang, S.W., Lee, S.H., Roh, H.S., Yang, S., Kurade, M.B., El-Dalatony, M.M., Kim, K.H., & Kim, S. (2017). Interactive effect of indole-3-acetic acid and diethyl aminoethyl hexanoate on the growth and fatty acid content of some microalgae for biodiesel production. Journal of Cleaner Production,168,1017–1024. DOI: https://doi.org/10.1016/j.jclepro.2017.09.057
  74. Sales, D.C., Rangel, A.H.N., Urbano, S.A., Freitas, A.R., Tonhati, H., Novaes, L.P., Pereira, M.I.B., & Borba, L.H.F. (2017). Relationship between mozzarella yield and milk composition, processing factors, and recovery of whey constituents. Journal of Dairy Science, 100, 4308–4321. DOI: https://doi.org/10.3168/jds.2016-12392
  75. Salla, A.C.V., Margarites, A.C., Seibel, F.I., Holz, L.C., Brião, V.B., Bertolin, T.E., Colla, L.M., & Costa, J.A.V. (2016). Increase in the carbohydrate content of the microalgae Spirulina in culture by nutrient starvation and the addition of residues of whey protein concentrate. Bioresource Technology,209, 133–141 DOI: https://doi.org/10.1016/j.biortech.2016.02.069
  76. Sarfraz, R., Taneez, M., Sardar, S., Danish, L. & Hameed, A. (2021). Evaluation of Desmodesmus subspicatus for the treatment of wastewater. International Journal of Environmental Analytical Chemistry. DOI: https://doi.org/10.1080/03067319.2021.1910681
  77. Seghiri, R., Kharbach, M., & Essamri, A. (2019). Functional Composition, Nutritional Properties, and Biological Activities of Moroccan Spirulina Microalga. Journal of Food Quality,2019,1-11. DOI: https://doi.org/10.1155/2019/3707219
  78. Sharoba, A.M. (2014). Nutritional value of spirulina and its use in the preparation of some complementary baby food formulas. Journal of Agroalimentary Processes and Technologies, 20, 330-350. DOI: https://doi.org/10.21608/jfds.2014.53033
  79. Sialve, B., Bernet, N., & Bernard, O. (2009). Anaerobic digestion of microalgae as a necessary step to make microalgal biodiesel sustainable. Biotechnology Advances, 27, 409–416. DOI: https://doi.org/10.1016/j.biotechadv.2009.03.001
  80. Soltani, N., Khavari-Nejad, R.A., Tabatabaei Yazdi, M., Shokravi, S.H. & Fernandez-Valiente, E. (2005). Screening of soil cyano bacteria for antibacterial antifungal activity. Pharmaceutical Biology, 43, 455-459. DOI: https://doi.org/10.1080/13880200590963871
  81. Sorokina, K.N., Samoylova, Y.V., & Parmon, V.N. (2020). Comparative analysis of microalgae metabolism on BBM and municipal wastewater during salt induced lipid accumulation. Bioresource Technology, 11, 1-12. DOI: https://doi.org/10.1016/j.biteb.2020.100548
  82. Taga, M.S., Miller, E.E., & Pratt, D.E. (1984). Chia seeds as a source of natural lipid antioxidants. Journal of American Oil Chemists’ Society, 61, 928-31. DOI: https://doi.org/10.1007/BF02542169
  83. Verma, A. & Singh, A. (2017). Physico-Chemical Analysis of Dairy Industrial Effluent. International Journal of Current Microbiology & Applied Sciences. 6, 1769-1775. DOI: https://doi.org/10.20546/ijcmas.2017.607.213
  84. World Health Organization (WHO) (1996). Permissible limits of heavy metals in soil and plants. Geneva, Switzerland.
  85. Wuang, S.C., Khin, M.C., Chua, P.Q.D. & Luo, Y.D. (2016). Use of Spirulina biomass produced from treatment of aquaculture wastewater as agricultural fertilizers. Algal Research, 15,59–64. DOI: https://doi.org/10.1016/j.algal.2016.02.009
  86. Yap, P.Y., Jain, A., & Trau, D. (2018). Tip Biosystems Pte Ltd, Singapore.
  87. Yen, G.C., & Chen, H.Y. (1995). Antioxidant activity of various tea extracts in relation to their antimutagenicity. Journal of Agricultural and Food Chemistry, 43, 27-32. DOI: https://doi.org/10.1021/jf00049a007
  88. Yousaf, S., Khan, S., Sher, H, Afridi, I. & Ahmad, D. (2013). Canal water treatment with rapid sand filtration. Soil Environment, 32, 103-107.
  89. Yu, F.R., Lian, X.Z., Guo, H.Y., McGuire, P.M., Li, R.D., Wang, R., & Yu, F.H. (2005). Isolation and characterization of methyl esters and derivatives from Euphorbia kansui (Euphorbiaceae) and their inhibitory effects on the human SGC-7901 cells. Journal of Pharmacy and Pharmaceutical Sciences, 8, 528-35.
  90. Yu, L., Li, X., Liu, S., Xu, G., & Liang, Y. (2009). Comparative analysis of volatile constituents in Citrus Reticulata Blanco using GC‒MS and alternative moving window factor analysis. Journal of Separation Science, 32, 3457-65. DOI: https://doi.org/10.1002/jssc.200900267
  91. Yuan, X., Kumar, A., Sahu, A.K., & Ergas, S.J. (2011). Impact of ammonia concentration on Spirulina platensis growth in an airlift photobioreactor. Bioresource Technology, 102, 3234–39. DOI: https://doi.org/10.1016/j.biortech.2010.11.019