Cite this paper:
Taha Mohamed EL-KATONY, Magda Faiz EL-ADL. Salt response of the freshwater microalga Scenedesmus obliquus (Turp.) Kutz is modulated by the algal growth phase[J]. HaiyangYuHuZhao, 2020, 38(3): 802-815

Salt response of the freshwater microalga Scenedesmus obliquus (Turp.) Kutz is modulated by the algal growth phase

Taha Mohamed EL-KATONY, Magda Faiz EL-ADL
Department of Botany and Microbiology, Faculty of Science, Damietta University, New Damietta City 34517, Egypt
Abstract:
Growth and biochemical responses of the coenobial green alga Scenedesmus obliquus to salinity stress were monitored across different phases of growth. The alga was cultured on BG11 growth medium and subjected to 0, 30, 100, and 200 mmol/L NaCl for a period of 20 d, during which algal cultures were harvested at 4-d intervals. The salinity-induced inhibition of algal growth was accompanied with prolongation of timing of the different growth phases. The sharp and progressive salinity-induced inhibition of algal growth rate during the early phase of growth points to salt shock but moderation of inhibition at the subsequent stages of growth means algal acclimation to salinity. The concentrations of chlorophylls a and b, soluble sugars, proteins as well as those of K+ and Na+ in the alga exhibited peaks at the initiation of the exponential phase of growth, with increasing magnitude in proportion to the increase in the level of salinity. Nevertheless, whereas soluble sugars of the alga peaked at initiation of the exponential phase, starch concentration progressively increased with culture age, reaching saturation towards the stationary phase. Whereas the salinity-induced increase in soluble sugars was most evident at the early stages of growth the reverse was true for starch. The present results point to fast acclimation of S. obliquus to salt stress post a brief salt shock, utilizing soluble sugars, K+ and Na+ for osmotic adjustment. Increasing salinity from 0 to 200 mmol/L NaCl led to progressive increase in soluble sugars, proteins, K+ and Na+ concentrations of the algal cells, particularly at the early stages of growth. However, the salinity-induced increase in chlorophyll concentration approached a limit at 100 mmol/L NaCl whereas that in starch concentration was more evident at the later stages of growth.
Key words:    carbohydrates|growth phase|minerals|protein|salt stress|Scenedesmus obliquus   
Received: 2019-03-14   Revised: 2019-07-02
Tools
PDF (921 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Taha Mohamed EL-KATONY
Articles by Magda Faiz EL-ADL
References:
Ahmed A M, Mohamed A A, Heikal M M, Shafea A A. 1989.Changes in metabolism of Scenedesmus obliquus after relief of salinization stress. Medical Journal of Islamic World Academy of Sciences, 2(2):100-105.
Ahmed R A, He M L, Aftab R A, Zheng S Y, Nagi M, Bakri R, Wang C H. 2017. Bioenergy application of Dunaliella salina SA 134 grown at various salinity levels for lipid production. Scientific Reports, 7(1):8 118, https://doi.org/10.1038/s41598-017-07540-x.
Akça Y, Samsunlu E. 2012. The effect of salt stress on growth, chlorophyll content, proline and nutrient accumulation, and K/Na ratio in walnut. Pakistan Journal of Botany, 44(5):1 513-1 520.
Alam A, Ullah S, Alam S, Shah H U, Aftab S, Siddiq M, Manzoor N. 2015. Influence of culture media and carbon sources on biomass productivity and oil content of the algae Sirogonium sticticum, Temnogyra reflexa, Uronema elongatum, and Chroococcus turgidus. Turkish Journal of Botany, 39(4):599-605, https://doi.org/10.3906/bot-1405-16.
BenMoussa-Dahmen I, Chtourou H, Rezgui F, Sayadi S, Dhouib A. 2016. Salinity stress increases lipid, secondary metabolites and enzyme activity in Amphora subtropica and Dunaliella sp. for biodiesel production. Bioresource Technology, 218:816-825, https://doi.org/10.1016/j.biortech.2016.07.022.
Bleakley S, Hayes M. 2017. Algal proteins:extraction, application, and challenges concerning production.Foods, 6(5):33, https://doi.org/10.3390/foods6050033.
Boland M J, Rae A N, Vereijken J M, Meuwissen M P M, Fischer A R H, Van Boekel M A J S, Rutherfurd S M, Gruppen H, Moughan P J, Hendriks W H. 2013. The future supply of animal-derived protein for human consumption. Trends in Food Science & Technology, 29(1):62-73, https://doi.org/10.1016/j.tifs.2012.07.002.
Bonomelli C, Celis V, Lombardi G, Mártiz J. 2018. Salt stress effects on avocado (Persea americana Mill.) plants with and without seaweed extract (Ascophyllum nodosum)application. Agronomy, 8(5):64, https://doi.org/10.3390/agronomy8050064.
Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2):248-254, https://doi.org/10.1016/0003-2697(76)90527-3.
Brányiková I, Maršálková B, Doucha J, Brányik T, Bišová K, Zachleder V, Vítová M. 2011. Microalgae-novel highly efficient starch producers. Biotechnology and Bioengineering, 108(4):766-776, https://doi.org/10.1002/bit.23016.
Chinnasamy S, Bhatnagar A, Hunt R W, Das K C. 2010.Microalgae cultivation in a wastewater dominated by carpet mill effluents for biofuel applications. Bioresource Technology, 101(9):3 097-3 105, https://doi.org/10.1016/j.biortech.2009.12.026.
Chiu L D, Ho S H, Shimada R, Ren N Q, Ozawa T. 2017.Rapid in vivo lipid/carbohydrate quantification of single microalgal cell by Raman spectral imaging to reveal salinity-induced starch-to-lipid shift. Biotechnology for Biofuels, 10:9, https://doi.org/10.1186/s13068-016-0691-y.
Church J, Hwang J H, Kim K T, McLean R, Oh Y K, Nam B, Joo J C, Lee W H. 2017. Effect of salt type and concentration on the growth and lipid content of Chlorella vulgaris in synthetic saline wastewater for biofuel production. Bioresource Technology, 243:147-153, https://doi.org/10.1016/j.biortech.2017.06.081.
Combres C, Laliberté G, Reyssac J S, De La Noüe J. 1994.Effect of acetate on growth and ammonium uptake in the microalga Scenedesmus obliquus. Physiologia Plantarum, 91(4):729-734, https://doi.org/10.1111/j.1399-3054.1994.tb03012.x.
De Vries S C, Van De Ven G W J, Van Ittersum M K, Giller K E. 2010. Resource use efficiency and environmental performance of nine major biofuel crops, processed by first-generation conversion techniques. Biomass and Bioenergy, 34(5):588-601, https://doi.org/10.1016/j.biombioe.2010.01.001.
Del Río E, García-Gómez E, Moreno J, Guerrero M G, GarcíaGonzález M. 2017. Microalgae for oil. Assessment of fatty acid productivity in continuous culture by two highyield strains, Chlorococcum oleofaciens and Pseudokirchneriella subcapitata. Algal Research, 23:37-42, https://doi.org/10.1016/j.algal.2017.01.003.
Elliott D C, Biller P, Ross A B, Schmidt A J, Jones S B. 2015.Hydrothermal liquefaction of biomass:developments from batch to continuous process. Bioresource Technology, 178:147-156, https://doi.org/10.1016/j.biortech.2014.09.132.
Erdmann N, Hagemann M. 2001. Salt acclimation of algae and cyanobacteria:a comparison. In:Rai L C, Gaur J P eds.Algal Adaptation to Environmental Stresses:Physiological, Biochemical and Molecular Mechanisms.Springer, Berlin, Heidelberg. p.323-361, https://doi.org/10.1007/978-3-642-59491-5_11.
García N, López-Elías J A, Miranda A, Martínez-Porchas M, Huerta N, García A. 2012. Effect of salinity on growth and chemical composition of the diatom Thalassiosira weissflogii at three culture phases. Latin American Journal of Aquatic Research, 40(2):435-440, https://doi.org/10.3856/vol40-issue2-fulltext-18.
Gu N, Lin Q, Li G, Tan Y H, Huang L M, Lin J D. 2012. Effect of salinity on growth, biochemical composition, and lipid productivity of Nannochloropsis oculata CS 179.Engineering in Life Sciences, 12(6):631-637, https://doi.org/10.1002/elsc.201100204.
Guiry M D, Guiry G M. 2013. AlgaeBase. World-wide Electronic Publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed on 2013.
Hansen E H, Munns D N. 1988. Effect of CaSO₄ and NaCl on mineral content of Leucaena leucocephala. Plant and Soil, 107(1):101-105, https://doi.org/10.1007/BF02371550.
Kaewkannetra P, Enmak P, Chiu T. 2012. The effect of CO2 and salinity on the cultivation of Scenedesmus obliquus for biodiesel production. Biotechnology and Bioprocess Engineering, 17(3):591-597, https://doi.org/10.1007/s12257-011-0533-5.
Khatoon H, Rahman N A, Banerjee S, Harun N, Suleiman S S, Zakaria N H, Lananan F, Abdul Hamid S H, Endut A. 2014. Effects of different salinities and pH on the growth and proximate composition of Nannochloropsis sp. and Tetraselmis sp. isolated from South China Sea cultured under control and natural condition. International Biodeterioration & Biodegradation, 95:11-18, https://doi.org/10.1016/j.ibiod.2014.06.022.
Kumari P, Kumar M, Reddy C R K, Jha B. 2014. Nitrate and phosphate regimes induced lipidomic and biochemical changes in the intertidal macroalga Ulva lactuca(Ulvophyceae, Chlorophyta). Plant and Cell Physiology, 55(1):52-63, https://doi.org/10.1093/pcp/pct156.
Lawton R J, De Nys R, Magnusson M E, Paul N A. 2015. The effect of salinity on the biomass productivity, protein and lipid composition of a freshwater macroalga. Algal Research, 12:213-220, https://doi.org/10.1016/j.algal. 2015.09.001.
Li Y Q, Horsman M, Wang B, Wu N, Lan C Q. 2008. Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Applied Microbiology and Biotechnology, 81(4):629-636, https://doi.org/10.1007/s00253-008-1681-1.
Maathuis F J M, Amtmann A. 1999. K+ Nutrition and Na+ toxicity:the basis of cellular K+/Na+ ratios. Annals of Botany, 84(2):123-133, https://doi.org/10.1006/anbo.1999.0912.
Moisander P H, McClinton E, Paerl H W. 2002. Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planktonic cyanobacteria. Microbial Ecology, 43(4):432-442, https://doi.org/10.1007/s00248-001-1044-2.
Pancha I, Chokshi K, Mishra S. 2015. Enhanced biofuel production potential with nutritional stress amelioration through optimization of carbon source and light intensity in Scenedesmus sp. CCNM 1077. Bioresource Technology, 179:565-572, https://doi.org/10.1016/j.biortech.2014.12.079.
Pandolfi C, Azzarello E, Mancuso S, Shabala S. 2016.Acclimation improves salt stress tolerance in Zea mays plants. Journal of Plant Physiology, 201:1-8, https://doi.org/10.1016/j.jplph.2016.06.010.
Park J B K, Craggs R J, Shilton A N. 2011. Wastewater treatment high rate algal ponds for biofuel production.Bioresource Technology, 102(1):35-42, https://doi.org/10.1016/j.biortech.2010.06.158.
Rai M P, Gautom T, Sharma N. 2015. Effect of salinity, pH, light intensity on growth and lipid production of microalgae for bioenergy application. OnLine Journal of Biological Sciences, 15(4):260-267, https://doi.org/10.3844/ojbsci.2015.260.267.
Schlüter U, Crawford R M M. 2001. Long-term anoxia tolerance in leaves of Acorus calamus L. and Iris pseudacorus L. Journal of Experimental Botany, 52(364):2 213-2 225, https://doi.org/10.1093/jexbot/52.364.2213.
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, 11:7, https://doi.org/10.1186/1472-6750-11-7.
Sudhir P, Murthy S D S. 2004. Effects of salt stress on basic processes of photosynthesis. Photosynthetica, 42(4):481-486.
Talebi A F, Mohtashami S K, Tabatabae M, Tohidfar M, Bagheri A, Zeinalabedini M, Mirzaei H H, Mirzajanzadeh M, Shafaroudi S M, Bakhtiari S. 2013. Fatty acids profiling:a selective criterion for screening microalgae strains for biodiesel production. Algal Research, 2(3):258-267, https://doi.org/10.1016/j.algal.2013.04.003.
Tang D H, Han W, Li P L, Miao X L, Zhong J J. 2011. CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresource Technology, 102(3):3 071-3 076, https://doi.org/10.1016/j.biortech.2010.10.047.
Tran H L, Kwon J S, Kim Z H, Oh Y, Lee C G. 2010. Statistical optimization of culture media for growth and lipid production of Botryococcus braunii LB572. Biotechnology and Bioprocess Engineering, 15(2):277-284, https://doi.org/10.1007/s12257-009-0127-7.
Wellburn A R, Lichtenthaler H. 1984. Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. In:Sybesma C ed.Advances in Photosynthesis Research. Springer, Dordrecht. p.9-12, https://doi.org/10.1007/978-94-017-6368-4_3.
Yamaguchi S, Motokura K, Tanaka K, Imamura S. 2017.Catalytic processes for utilizing carbohydrates derived from algal biomass. Catalysts, 7(5):163, https://doi.org/10.3390/catal7050163.
Yang Y Q, Guo Y. 2018. Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytologist, 217(2):523-539, https://doi.org/10.1111/nph.14920.