Growth and biochemical profiling of marine microalgae Chlorella salina with response to nitrogen starvation

References

• Adams C, Godfrey V, Wahlen B, Seefeldt L, Bugbee B. 2013. Understanding precision nitrogen stress to optimize the growth and lipid content tradeoff in oleaginous green microalgae. Bioresource Technology. 131:188–194. doi:10.1016/j.biortech.2012.12.143
   PubMed Web of Science ®Google Scholar
• Babu GA, Wu X, Kabra AN, Kim DP. 2017. Cultivation of an indigenous Chlorella sorokiniana with phytohotmones for biomass and lipid production under N-limitation. Algal Research. 23:178–185. doi:10.1016/j.algal.2017.02.004
   Google Scholar
• Becker W. 2004. Microalgae in human and animal nutrition. In: Richmond A, editor. Handbook of microalgal culture. New York: Applied Phycology and Biotechnology; p. 312–351.
   Google Scholar
• Benvenuti G, Bosma R, Cuaresma M, Janssen M, Barbosa MJ, Wijffels RH. 2015. Selecting microalgae with high lipid productivity and photosynthetic activity under nitrogen starvation. Journal of Applied Phycology. 27:1425–1431. doi:10.1007/s10811-014-0470-8
   Web of Science ®Google Scholar
• Brown MR. 1991. The amino-acid and sugar composition of 16 species of microalgae used in mariculture. Journal of Experimental Marine Biology and Ecology. 145(1):79–99. doi:10.1016/0022-0981(91)90007-J
   Web of Science ®Google Scholar
• Collin AM, Jones HD, Han D, Hu Q, Beechem TE, Timlin JA. 2011. Carotenoid distribution in living cells of haematococcuspluvialis (chlorophyceae). PLoS One. 6(9):1–7. doi:10.1371/journal.pone.0024302
   Web of Science ®Google Scholar
• Day JG, Slocombe SP, Stanley MS. 2012. Overcoming biological constraints to enable the exploitation of microalgae for biofuels. Bioresource Technology. 109:245–251. doi:10.1016/j.biortech.2011.05.033
   PubMed Web of Science ®Google Scholar
• de la Rocha SRF, Muniz JS, Juaristi MG, Marín MTL. 2009. Trace elements determination in edible seaweeds by an optimized and validated ICP-MS method. Journal of Food Composition and Analysis. 22:330–336. doi:10.1016/j.jfca.2008.10.021
   Web of Science ®Google Scholar
• Del Campo JA, Garcia-Gonzalez M, Guerrero MG. 2007. Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Applied Microbiology and Biotechnology. 74:1163–1174. doi:10.1007/s00253-007-0844-9
   PubMed Web of Science ®Google Scholar
• Devi GK, Thirumaran G, Manivannan K, Anantharaman P. 2009. Element composition of certain seaweeds from Gulf of Mannar marine biosphere reserve; Southeast coast of India. World Journal of Dairy Food Science. 4:46–55.
   Google Scholar
• Dillschneider R, Steinweg C, Rosello-Sastre R, Posten C. 2013. Biofuels from microalgae: photoconversion efficiency during lipid accumulation. Bioresource Technology. 142:647–654. doi:10.1016/j.biortech.2013.05.088.
   PubMed Web of Science ®Google Scholar
• Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry. 28:350–356. doi:10.1021/ac60111a017
   Web of Science ®Google Scholar
• Fidalgo JP, Cid A, Torres E, Sukenik A, Herrero C. 1998. Effects of nitrogen source and growth phase on proximate biochemical composition, lipid classes and fatty acid profile of the marine microalga Isochrysis galbana. Aquaculture. 166(1-2):105–116. doi:10.1016/S0044-8486(98)00278-6
   Web of Science ®Google Scholar
• Folch J, Lees M, Stanley GS. 1957. A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry. 226(1):497–509. doi:10.1016/S0021-9258(18)64849-5
   PubMed Web of Science ®Google Scholar
• Geider RJ, MacIntyre HL, Kana TM. 1997. Dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and the chlorophyll a: carbon ratio to light, nutrient-limitation and temperature. Marine Ecology Progress Series. 148:187–200. doi:10.3354/meps148187.
   Web of Science ®Google Scholar
• Griffiths MJ, van Hille RP, Harrison ST. 2014. The effect of nitrogen limitation on lipid productivity and cell composition in Chlorella vulgaris. Applied Microbiology and Biotechnology. 98:2345–2356. doi:10.1007/s00253-013-5442-4.
   PubMed Web of Science ®Google Scholar
• Grima EM, Belarbi EH, Fernández FGA, Medina AR, Chisti Y. 2003. Recovery of microalgal biomass and metabolites: process options and economics. Biotechnology Advances. 20:491–515. doi:10.1016/S0734-9750(02)00050-2
   PubMed Web of Science ®Google Scholar
• Guccione A, Biondi N, Sampietro G, Rodolfi L, Bassi N, Tredici MR. 2014. Chlorella for protein and biofuels: from strain selection to outdoor cultivation in a Green Wall Panel photobioreactor. Biotechnology for Biofuels. 7:1–12. doi:10.1186/1754-6834-7-84.
   PubMed Web of Science ®Google Scholar
• Guihéneuf F, Stengel DB. 2015. Towards the biorefinery concept: interaction of light, temperature and nitrogen for optimizing the co-production of high-value compounds in Porphyridium purpureum. Algal Research. 10:152–163. doi:10.1016/j.algal.2015.04.025
   Google Scholar
• Heraud P, Wood BR, Beardall J, McNaughton D. 2006. Effects of pre-processing of Raman spectra on in vivo classification of nutrient status of microalgal cells. Journal of Chemometrics. 20(5):193–197. doi:10.1002/cem.990
   Web of Science ®Google Scholar
• Ho SH, Chen CY, Chang JS. 2012. Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresource Technology. 113:244–252. doi:10.1016/j.biortech.2011.11.133
   PubMed Web of Science ®Google Scholar
• Ho SH, Huang SW, Chen CY, Hasunuma T, Kondo A, Chang JS. 2013. Characterization and optimization of carbohydrate production from an indigenous microalga Chlorella vulgaris FSP-E, Bioresour. Technol. 135:157–165.
   Google Scholar
• Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A. 2008. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. The Plant Journal. 54(4):621–639. doi:10.1111/j.1365-313X.2008.03492.x
   PubMed Web of Science ®Google Scholar
• Jiang Y, Yoshida T, Quigg A. 2012. Photosynthetic performance, lipid production and biomass composition in response to nitrogen limitation in marine microalgae. Plant Physiology and Biochemistry. 54:70–77. doi:10.1016/j.plaphy.2012.02.012
   PubMed Web of Science ®Google Scholar
• Kilham S, Kerrger D, Goulden C, Lynn S. 1997. Effects of nutrient limitation on biochemical constituents of Ankistrodesmus falcatus. Freshwater Biology. 38(3):591–596. doi:10.1046/j.1365-2427.1997.00231.x
   Web of Science ®Google Scholar
• Kliphuis AM, Klok AJ, Martens DE, Lamers PP, Janssen M, Wijffels RH. 2012. Metabolic modeling of Chlamydomonas reinhardtii: energy requirements for photoautotrophic growth and maintenance. Journal of Applied Phycology. 24:253–266. doi:10.1007/s10811-011-9674-3.
   PubMed Web of Science ®Google Scholar
• Li Z, Wakao S, Fischer BB, Niyogi KK. 2009. Sensing and responding to excess light. Annual Review of Plant Biology. 60:239–260. doi:10.1146/annurev.arplant.58.032806.103844
   PubMed Web of Science ®Google Scholar
• Lin Y-H, Chang F-L, Tsao C-Y, Leu J-Y. 2007. Influence of growth phase and nutrient source on fatty acid composition of Isochrysis galbana CCMP 1324 in a batch photoreactor. Biochemical Engineering Journal. 37(2):166–176. doi:10.1016/j.bej.2007.04.014
   Web of Science ®Google Scholar
• Marín MTL, Alfonso MSP, Juaristi MG, Muniz FJS, de la Rocha SR. 2010. Validation of an ICP-OES method for macro and trace element determination in Laminaria and Porphyra seaweeds from four different countries. Journal of Food Composition and Analysis. 23:814–820. doi:10.1016/j.jfca.2010.03.015
   Web of Science ®Google Scholar
• Moreno-Garcia L, Adjallé K, Barnabé S, Raghavan GSV. 2017. Microalgae biomass production for a biorefinery system: recent advances and the way towards sustainability. Renewable and Sustainable Energy Reviews. 76:493–506. doi:10.1016/j.rser.2017.03.024
   Web of Science ®Google Scholar
• Pancha I, Ghosh A, Mishra S. 2017. Salinity induced oxidative stress alters the physiological responses and improves the biofuel potential of green microalgae Acutodesmus dimorphus. Bioresource Technology. 244:1376–1383. doi:10.1016/j.biortech.2017.05.003
   PubMed Web of Science ®Google Scholar
• Panis G, Carreon JR. 2016. Commercial astaxanthin production derived by green alga Haematococcus pluvialis: a microalgae process model and a techno-economic assessment all through production line. Algal Research. 18:175–190. doi:10.1016/j.algal.2016.06.007
   Google Scholar
• Piorreck M, Baasch KH, Pohl P. 1984. Biomass production, total protein, chlorophylls, lipids and fatty acids of freshwater green and blue-green algae under different nitrogen regimes. Phytochemistry. 23:207–216. DOI: 10.1016/S0031-9422(00)80304-0.
   Web of Science ®Google Scholar
• Rajendran N, Karpanai Selvan B, SobanaPiriya P, Logeswari V, Kathiresan E, Tamilselvi A, John Vennison S. 2014. Phytochemicals, antimicrobial and antioxidant screening from five different marine microalgae. Journal of Chemical and Pharmaceutical Sciences. 7(2):78–85.
   Google Scholar
• Shah M, Mahfuzur R, Liang Y, Cheng JJ, Daroch M. 2016. Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Frontiers in Plant Science. 7:1–28.
   PubMed Web of Science ®Google Scholar
• Shams El Din NG, El-Sherif. ZM. 2012. Nutritional value of some algae from the north-western Mediterranean Coast of Egypt. Journal of Applied Phycology. 24:613–626. doi:10.1007/s10811-012-9831-3
   Web of Science ®Google Scholar
• Solovchenko AE. 2013. Physiology and adaptive significance of secondary carotenogenesis in green microalgae. Russian Journal of Plant Physiology. 60(1):1–13. doi:10.1134/S1021443713010081
   Web of Science ®Google Scholar
• Śmieszek A, Giezek E, Chrapiec M, Murat M, Mucha A, Michalak I, Marycz K. 2017. The influence of Spirulina platensis filtrates on Caco-2 proliferative activity and expression of apoptosis-related microRNAs and mRNA. Marine Drugs. 15(3):1–18. doi:10.3390/md15030065
   Web of Science ®Google Scholar
• Tao L, Linglin W, Aifen L, Chengwu Z. 2013. Responses in growth, lipid accumulation, and fatty acid composition of four oleaginous microalgae to different nitrogen sources and concentrations. Chinese Journal of Oceanology and Limnology. 31:1306–1314. doi:10.1007/s00343-013-2316-7
   Web of Science ®Google Scholar
• Tompkins J, DeVille MM, Day JG, Turner MF. 1995. Culture collection of algae and protozoa catalogue of strains. 6th ed. Ambleside: Culture Collection of Algae and Protozoa; p. 208.
   Google Scholar
• Wang HT, Yao CH, Ai JN, Cao XP, Xue S, Wang WL. 2014. Identification of carbohydrates as the major carbon sink of the marine microalga Isochrysis zhangjiangensis (Haptophyta) and optimization of its productivity by nitrogen manipulation. Bioresource Technology. 171:298–304. doi:10.1016/j.biortech.2014.08.090
   PubMed Web of Science ®Google Scholar
• Wang J, Yang H, Wang F. 2014. Mixotrophic cultivation of microalgae for biodiesel production: status and prospects. Applied Biochemistry and Biotechnology. 172:3307–3329. doi:10.1007/s12010-014-0729-1
   PubMed Web of Science ®Google Scholar
• Wellburn AR. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology. 144(3):307–313. doi:10.1016/S0176-1617(11)81192-2
   Web of Science ®Google Scholar
• Zhang L, Liu J. 2016. Enhanced fatty acid accumulation in Isochrysis galbana by inhibition of the mitochondrial alternative oxidase pathway under nitrogen deprivation. Bioresource Technology. 211:783–786. doi:10.1016/j.biortech.2016.03.164
   PubMed Web of Science ®Google Scholar