Present study showed that the higher growth rate, biomass, and protein content were directly related with the higher nitrogen concentration in the culture condition. Hence, it is recommended that Nannochloropsis sp. should be cultured in higher nitrogen concentration for achieving higher biomass in terms of growth and protein content.
Present study also revealed that the lower nitrogen concentration in the culture media induced the accumulation of higher lipid in the cell. Therefore, Nannochloropsis sp.
need to culture in the depleted nitrogen concentration to get higher lipid. Though protein content was higher in higher nitrogen concentration, the quality of protein cannot predict from this study. In addition, the higher lipid content cannot be an indicator of good quality lipid. The protein quality and lipid quality could be assured by the determination of amino acid and fatty acid profile. Future research need to be done on the determination of fatty acids and amino acids profile.
38 References
Abadia, J. 1986. Function of iron in chloroplasts. Journal of Plant Nutrition. 9(3–7):
609–646.
Agarwal, A., Xu, T., Jacob, M., Feng, Q., Li, X., Walker, L., & Clark, A. 2012.
Genomic and Genetic Approaches for the Identification of Antifungal Drug Targets. Infectious Disorders - Drug Targets.8(1): 2–15.
Angles, E., Jaouen, P., Pruvost, J., & Marchal, L. 2017. Wet lipid extraction from the microalga Nannochloropsis sp.: Disruption, physiological effects and solvent screening. Algal Research, 21, pp. 27–34.
Bartley, M. L., Boeing, W. J., Corcoran, A. A., Holguin, F. O., & Schaub, T. 2013.
Effects of salinity on growth and lipid accumulation of biofuel microalga Nannochloropsis salina and invading organisms. Biomass and Bioenergy, 54, pp. 83–88.
Béchet, Q., Shilton, A., Fringer, O. B., Munoz, R., & Guieysse, B. 2010. Mechanistic modeling of broth temperature in outdoor photobioreactors.Environmental Science and Technology, 44(6), 2197–2203.
Bellou, S., Triantaphyllidou, I. E., Aggeli, D., Elazzazy, A. M., Baeshen, M. N., &
Aggelis, G. 2016. Microbial oils as food additives: Recent approaches for improving microbial oil production and its polyunsaturated fatty acid content.
Current Opinion in Biotechnology, 37, pp. 24–35.
Benvenuti, G., Lamers, P. P., Breuer, G., Bosma, R., Cerar, A., Wijffels, R. H.,
&Barbosa, M. J. 2016. Microalgal TAG production strategies: Why batch beats repeated-batch. Biotechnology for Biofuels, 9(1), 1–17.
Brown, M. R., Jeffrey, S. W., Volkman, J. K., & Dunstan, G. A. 1997. Nutritional properties of microalgae for mariculture. Aquaculture, 151(1–4), 315–331.
Bruland, K. W., Donat, J. R., & Hutchins, D. A. 1991. Interactive influences of bioactive trace metals on biological production in oceanic waters.Limnology and Oceanography, 36(8), 1555–1577.
Bryant, H. L., Richardson, J. W., Wickersham, T. A., Maisashvili, A., Bryant, H., Richardson, J., Anderson, D., Wickersham, T., & Drewery, M. 2001.The values of whole algae and lipid extracted algae meal for aquaculture. 27, pp. 218-222
39
Chauton, M. S., Reitan, K. I., Norsker, N. H., Tveterås, R., & Kleivdal, H. T. 2015. A techno-economic analysis of industrial production of marine microalgae as a source of EPA and DHA-rich raw material for aquafeed: Research challenges and possibilities. Aquaculture, 436,pp. 95–103.
Chisti, Y. 2007. Biodiesel from microalgae.Biotechnology Advances, 25(3), 294–306.
Converti, A., Casazza, A. A., Ortiz, E. Y., Perego, P., & Del Borghi, M. 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: Process Intensification, 48(6), 1146–
1151.
Cuhel, R. L., Ortner, P. B., & Lean, D. R. S. 1984. Night synthesis of protein by algae.
Limnology and Oceanography, 29(4), 731–744.
D’Souza, F. M. L., & Kelly, G. J. 2000. Effects of a diet of a nitrogen-limited alga (Tetraselmis suecica) on growth, survival and biochemical composition of tiger prawn (Penaeus semisulcatus) larvae.Aquaculture, 181(3–4), 311–329.
El-Kassas, H. Y. 2013. Growth and fatty acid profile of the marine microalga Picochlorum Sp. grown under nutrient stress conditions. Egyptian Journal of Aquatic Research, 39(4), 233–239.
Greene, R. M., Geider, R. J., Kolber, Z., & Falkowski, P. G. 1992. Iron-induced changes in light harvesting and photochemical energy conversion processes in eukaryotic marine algae. Plant Physiology, 100(2), 565–575.
Günerken, E., D’Hondt, E., Eppink, M., Elst, K., & Wijffels, R. 2016. Influence of nitrogen depletion in the growth of N. oleoabundans on the release of cellular components after beadmilling. Bioresource Technology, 214, pp. 89–95.
Harrison, P. J. 2014. Marine Culture Media. February 2005, pp. 21–33.
Ho, S. H., Chen, C. Y., & Chang, J. S. 2012. Effect of light intensity and nitrogen starvation on CO 2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresource Technology, 113, pp.
244–252.
Ho, S. H., Chen, C. Y., Lee, D. J., & Chang, J. S. 2011. Perspectives on microalgal CO2-emission mitigation systems - A review.Biotechnology Advances, 29(2),
40 189–198.
Hu, H., & Gao, K. 2003. Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. In Biotechnology Letters 25, pp.89-92
Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., & Darzins, A. 2008a. Microalgal triacylglycerols as feedstocks for biofuel production:
Perspectives and advances. Plant Journal, 54(4), 621–639.
Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., & Darzins, A. 2008b. Microalgal triacylglycerols as feedstocks for biofuel production:
Perspectives and advances.Plant Journal , 54(4), 621–639.
Huo, Y. X., Cho, K. M., Rivera, J. G. L., Monte, E., Shen, C. R., Yan, Y., & Liao, J. C.
2011. Conversion of proteins into biofuels by engineering nitrogen flux.Nature Biotechnology, 29(4), 346–351.
Illman, A. M., Scragg, A. H., & Shales, S. W. 2000. Increase in Chlorella strains calorific values when grown in low nitrogen medium. Enzyme and Microbial Technology, 27(8), 631–635.
Ishika, T., Bahri, P. A., Laird, D. W., & Moheimani, N. R. 2018. The effect of gradual increase in salinity on the biomass productivity and biochemical composition of several marine, halotolerant, and halophilic microalgae. Journal of Applied Phycology, 30(3), 1453–1464.
Kagan, M. L., West, A. L., Zante, C., & Calder, P. C. 2013. Acute appearance of fatty acids in human plasma - A comparative study between polar-lipid rich oil from the microalgae Nannochloropsis oculata and krill oil in healthy young males.
Lipids in Health and Disease, 12(1), 1–10.
Kobayashi, M., Kakizono, T., & Nagai, S. 1993. Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Applied and Environmental Microbiology, 59(3), 867–873.
Lam, M. K., Yusoff, M. I., Uemura, Y., Lim, J. W., Khoo, C. G., Lee, K. T., & Ong, H.
C. 2017. Cultivation of Chlorella vulgaris using nutrients source from domestic wastewater for biodiesel production: Growth condition and kinetic studies.
41 Renewable Energy, 103, pp.197–207.
Larned, S. T. 1998. Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Marine Biology, 132(3), 409–421.
Laura Barsanti, P. G. 2006. Algae: Anatomy, Biochemistry, and Biotechnology, Second Edition - 2nd. Algae - Anatomy, Biochemistry and Biotechnology,.
Leyva, L. A., Bashan, Y., Mendoza, A., & de-Bashan, L. E. 2014. Accumulation fatty acids of in Chlorella vulgaris under heterotrophic conditions in relation to activity of acetyl-CoA carboxylase, temperature, and co-immobilization with Azospirillum brasilense. Die Naturwissenschaften, 101(10), 819–830.
Li, Q., Du, W., & Liu, D. 2008. Perspectives of microbial oils for biodiesel production.
Applied Microbiology and Biotechnology, 80(5), 749–756.
Liu, Z. Y., Wang, G. C., & Zhou, B. C. 2008. Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresource Technology, 99(11), 4717–
4722.
Ma, S., Han, B., Huss, V. A. R., Hu, X., Sun, X., & Zhang, J. 2015. Chlorella thermophila (Trebouxiophyceae, Chlorophyta), a novel thermo-tolerant Chlorella species isolated from an occupied rooftop incubator. Hydrobiologia, 760(1), 81–89.
Mai, T., Nguyen, P., Vo, T., Huynh, H., Tran, S., Nim, T., Tran, D., Nguyen, H., &
Bui, P. 2017. Accumulation of lipid in Dunaliella salina under Nutrient Starvation Condition. American Journal of Food and Nutrition, 5(2), 58–61.
Mata, T. M., Martins, A. A., & Caetano, N. S. 2010. Microalgae for biodiesel production and other applications: A review.Renewable and Sustainable Energy Reviews, 14(1), 217–232.
Mühlroth, A., Li, K., Røkke, G., Winge, P., Olsen, Y., Hohmann-Marriott, M. F., Vadstein, O., & Bones, A. M. 2013. Pathways of lipid metabolism in marine algae, co-expression network, bottlenecks and candidate genes for enhanced production of EPA and DHA in species of chromista.Marine Drugs11(11),4662–4697).
Mar Drugs.Navarro-Peraza, R. S., Piña-Valdez, P., Cuevas-Rodriguez, E. O., Nieves- Soto, M., Soto-León, S., Contreras-Andrade, I., & Viveros-García, T. 2017.
42
Effects of temperature and nitrogen limitation on growth kinetics, proximate composition and fatty acid profile of Nannochloropsis sp. Revista Mexicana de Ingeniera Quimica, 16(2), 359–369.
Norambuena, F., Hermon, K., Skrzypczyk, V., Emery, J. A., Sharon, Y., Beard, A., &
Turchini, G. M. 2015. Algae in fish feed: Performances and fatty acid metabolism in juvenile Atlantic Salmon. PLoS ONE, 10(4), 1–17.
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. CCNM 1077. Bioresource Technology, 156, pp.146–154.
Rao, A. R., Dayananda, C., Sarada, R., Shamala, T. R., & Ravishankar, G. A. 2007.
Effect of salinity on growth of green alga Botryococcus braunii and its constituents. Bioresource Technology, 98(3), 560–564.
Reitan, K. I., Rainuzzo, J. R., Øie, G., & Olsen, Y. 1997. A review of the nutritional effects of algae in marine fish larvae. Aquaculture, 155(1–4), 207–221.
Reitan, K. I., Rainuzzo, J. R., & Olsen, Y. 1994. Effect of Nutrient Limitationn on Fatty Acid andd Lipid Content of Marine Microalgae. Journal of Phycology, 30(6), 972–979.
Rismani-Yazdi, H., Haznedaroglu, B. Z., Bibby, K., & Peccia, J. 2011. Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: Pathway description and gene discovery for production of next-generation biofuels.
BMC Genomics, 12(1), 148.
Rodolfi, L., Zittelli, G. C., Bassi, N., Padovani, G., Biondi, N., Bonini, G., & Tredici, M. R. 2009. Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnology and Bioengineering, 102(1), 100–112.
Rosli, S. S., Lim, J. W., Uemura, Y., Lam, M. K., Isa, M. H., Oh, W. Da, & Sakidin, H.
2018. PH optimization to promote attached growth of microalgae biomass onto polyurethane foam material. AIP Conference Proceedings, 2016, pp.1–6.
Sabaté, J., & Soret, S. 2014. Sustainability of plant-based diets: back to the future. The American Journal of Clinical Nutrition, 100,pp.476S-482S.
43
Sato, N., Hagio, M., Wada, H., & Tsuzuki, M. 2000. Environmental effects on acidic lipids of thylakoid membranes. Biochemical Society Transactions.28(6): 912–
914.
Seto A, Kumasaka K, Hosaka M, Kojima E, Kashiwakura M, K. T. 1992. Production of eicosapentaenoic acid by a marine microalgae and its commercial utilization for aquaculture. In Kyle DJ, Ratledge C (eds), Industrial Applications of Single Cell Oils. American Oil Chemical Social Champaign, Illinois.pp. 219–234.
Shetty, P., Gitau, M. M., & Maróti, G. (2019). Salinity Stress Responses and Adaptation Mechanisms in Eukaryotic Green Microalgae. Cells, 8(12), 1–16.
Siaut, M., Cuiné, S., Cagnon, C., Fessler, B., Nguyen, M., Carrier, P., Beyly, A., Beisson, F., Triantaphylidès, C., Li-Beisson, Y., & Peltier, G. 2011. Oil accumulation in the model green alga Chlamydomonas reinhardtii:
Characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnology, 11(1), 7.
Solovchenko, A. E., Khozin-Goldberg, I., Didi-Cohen, S., Cohen, Z., & Merzlyak, M.
N. 2008. Effects of light intensity and nitrogen starvation on growth, total fatty acids and arachidonic acid in the green microalga Parietochloris incisa. Journal of Applied Phycology, 20(3), 245–251.
Spilling, K., Brynjólfsdóttir, Á., Enss, D., Rischer, H., & Svavarsson, H. G. 2013. The effect of high pH on structural lipids in diatoms. Journal of Applied Phycology, 25(5), 1435–1439.
Sukenik, A., &Carmeli, Y. 1990. Lipid synthesis and fatty acid composition in Nannochloropsis sp. ( Eustigmatophyceae) grown in light-drak cycle.Journal of Phycology, 26(3), 463–469.
Thompson, G. A. 1996. Lipids and membrane function in green algae. Biochimica et Biophysica Acta. 1302, pp. 114-117.
Turpin, D. H. 1991. Effects of inorganic N in availability on algal photosynthesis and carbon metabolism.Journal of Phycology, 27(1), 14–20.
Van Leeuwe, M. A., & Stefels, J. 1998. Effects of iron and light stress on the biochemical composition of antarctica Phaeocystis ( Prymnesiophyceae)pigment composition.Journal of Phycology, 34(3), 496–503.
44
Vymazal, J. 1988. The use of periphyton communities for nutrient removal from polluted streams. Hydrobiologia, 166(3), 225–237.
Wells, M. L., Potin, P., Craigie, J. S., Raven, J. A., Merchant, S. S., Helliwell, K. E., Smith, A. G., Camire, M. E., & Brawley, S. H. 2017. Algae as nutritional and functional food sources: revisiting our understanding. Journal of Applied Phycology 29(2), 949–982.
Westhoek, H., Lesschen, J. P., Rood, T., Wagner, S., De Marco, A., Murphy-Bokern, D., Leip, A., van Grinsven, H., Sutton, M. A., & Oenema, O. 2014. Food choices, health and environment: Effects of cutting Europe’s meat and dairy intake. Global Environmental Change, 26(1), 196–205.
Williams, P. J. L. B., & Laurens, L. M. L. 2010. Microalgae as biodiesel & biomass feedstocks: Review & analysis of the biochemistry, energetics & economics.
Energy and Environmental Science 3(5),554–590.
Xie, T., Xia, Y., Zeng, Y., Li, X., & Zhang, Y. 2017. Nitrate concentration-shift cultivation to enhance protein content of heterotrophic microalga Chlorella vulgaris: Over-compensation strategy. Bioresource Technology, 233, pp.247–
255.
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.
45