The effect of salinity, UV-C, UV-B irradiation stress on the growth, fatty acid and lipid class composition in Dunaliella salina

Document Type : Original Article

Authors

1 Department of Biology, Faculty of Sciences, Urmia University, Urmia, Iran.

2 Artemia & Aquaculture Research Institute, Urmia University, Urmia, Iran.

3 Department of Marine Biology, Tarbiat Modares University, Tehran, Iran.

Abstract

Dunaliella salina microalgae is a unique eukaryotic microorganism that has a high range of tolerance against environmental fluctuations including salinity, temperature, and light. The aim of this study was to determine the growth factors and content of fatty acids in D. salina under salinity and ultraviolet conditions. The experiments were conducted at three different salinities (150, 200 and 250 ppt) under UVB and UVC irradiations in 3 replicates. Algae growth rate and total algae biomass were measured by counting the number of cells every alternate day for 11 days by hemacytometer. The fatty acids profile was measured by gas chromatography and the amount of total fat using a soxhlet device. The growth rate of algae in most of the treatments under high salinity stress, UVB and UVC irradiation was significantly lower compared to the control group (P≤0.05). The highest cell counts were detected in the control one (2.4 million cells/ml) and UVB-150 treatment (1.98 million cells/ml) on day 7. But despite the higher cell count in the control group, the highest fresh wet weight of algae was obtained in the UVC-200 ppt/salinity group. Substantial differences were detected in the fatty acids profile between the treatments (P≤0.05). Algae cultured under UVB-200 contained the highest PUFA-n3 (20.05%) and the sum of PUFA (32.05%), while the highest PUFA-n6 (13.96%) was found in the UVC-150 group. Algae cultured at 250 ppt salinity without UV irradiation had the highest level (52.75%) of saturated fatty acids (SFA). It was concluded that UV irradiations and high salinity suppresses the growth but improves the synthesis of polyunsaturated fatty acids.

Keywords

References

Ahmed F., Zhou W., Schenk P.M. 2015. Pavlova lutheri is a high-level producer of phytosterols. Algal Research 10(4), 210-217.
Anand V., Kashyap M., Samadhiya K., Ghosh A., Kiran B. 2019. Salinity driven stress to enhance lipid production in Scenedesmus vacuolatus: a biodiesel trigger? Biomass Bioenergy 127(4), 105252.
Azachi M., Sadka A., Fisher M., Goldshlag P., Gokhman I., Zamir A. 2002. Salt induction of fatty acid elongase and membrane lipid modifications in the extreme halotolerant alga Dunaliella salina. Plant physiology 129(3), 1320-1329.
Bai X., Naghdi F.G., Ye L., Lant P., Pratt S. 2014. Enhanced lipid extraction from algae using free nitrous acid pretreatment. Bioresource Technology 159(4), 36-40.
Christov C., Pouneva I., Bozhkova M., Toncheva T., Founadzieva S., Zafirova T. 2001. Influence of temperature and methyl jasmonate on Scenedesmus uncrassulantus. Biologia Plantarum 44(3), 367-371.
Dhanam D.S., Dhandayuthapani K. 2013. Original Research Article Optimization of-Carotene production by Marine Microalga-Dunaliella salina. International Journal of Current Microbiology and Applied Sciences 2(3), 37-43.
FAO. 2007. Manual on the production and use of Live Food for Aquaculture. New York, UN. 361 p.
Faruq A., Peer M. 2017. UV-C radiation increases sterol production in the microalga Pavlova luthier. Phytochemistry 139(4), 25-32.
Fazeli M.R., Tofighi H., Samadi N., Jamalifar H., Fazeli A. 2006. Carotenoids accumulation by Dunaliella tertiolecta (Lake Urmia isolate) and Dunaliella salina (ccap 19/18 and wt) under stress conditions. DARU Journal of Pharmaceutical Sciences 14(3), 146-150.
Fisher M., Pick U., Zamir A. 1994. A salt-induced 60-kilodalton plasma membrane protein plays a potential role in the extreme halotolerance of the alga Dunaliella, Journal of Plant Physiology 106(4), 1359-1365.
Gaubert J., Payri C.E., Vieira C., Solanki H., Thomas O.P. 2019. High metabolic variation for seaweeds in response to environmental changes: a case study of the brown algae Lobophora in coral reefs. Scientific Reports 993(9), 1-12.
Gogna M., Choudhary A., Mishra G., Kapoor R., Bhatla S.C. 2020. Changes in lipid composition in response to salt stress and its possible interaction with intracellular Na‏-K ‏ ratio in sunflower Helianthus annuus L. Environmental and Experimental Botany 20(5), 104-147
Gogna M., Choudhary A., Mishra G., Kapoor R., Bhatla S.C. 2021. Changes in lipid composition in response to salt stress and its possible interaction with intracellular Naþ-K þ ratio in sunflower Helianthus annuus L. EnvironEnvironmental and Experimental Botany 178(5):104147
Goyal A. 2007. Osmoregulation in Dunaliella, Part I: Effects of osmotic stress on photosynthesis, dark respiration, and glycerol metabolism in Dunaliella tertiolecta and its salt-sensitive mutant (HL 25/8). Plant Physiology and Biochemistry  45(2), 696-704.
He M., Ding N.Z. 2020. Plant unsaturated fatty acids: multiple roles in stress response. Front. Plant Science 11(9), 1-15.
He Y.Y., Hader D.P. 2002. UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-L-cysteine. Journal of Photochemistry and Photobiology B: Biology 66(2), 115-124.
Hejazi M., Wijffels R. 2003. Effect of light intensity on β-carotene production and extraction by Dunaliella salina in two-phase bioreactors. Biomolecular Engineering 20(6), 171-175.
Hounslow E., Evans C.A., Pandhal J., Sydney T., Couto N., Pham T.K., Gilmour D.J., Wright P.C. 2021. Quantitative proteomic comparison of salt stress in Chlamydomonas reinhardtii and the snow alga Chlamydomonas nivalis reveals mechanisms for salt-triggered fatty acid accumulation via reallocation of carbon resources. Biotechnol. Biofuels 14(1), 1-25.
Huang J.J.H., Cheung P.C. K., 2011. UV-A treatment increases the degree of unsaturation in microalgal fatty acids and total carotenoid content in Nitzschia closterium (Bacillariophyceae) and Isochrysis zhangjiangensis (Chrysophyceae). Food Chemistry Journal 129(3), 783-791.
Huerlimann R., De Nys R., Heimann K. 2010. Growth, lipid content, productivity, and fatty acid composition of tropical microalgae for scale-up production. Biotechnology and Bioengineering 107(2), 245-257.
Ismaiel M.M.S., Piercey-Normore M.D., Rampitsch C. 2018. Proteomic analyses of the cyanobacterium Arthrospira (Spirulina) platensis under iron and salinity stress. Environmental and Experimental Botany 147(3), 63-74.
Ji C., Mao X., Hao J., Wang X., Xue J., Cui H., Li R. 2018a. Analysis of bZIP transcription factor family and their expressions under salt stress in Chlamydomonas reinhardtii. International Journal of Molecular Sciences 19(1), 1-19.
Ji X., Cheng J., Gong D., Zhao X., Qi Y., Su Y., Ma W. 2018b. The effect of NaCl stress on photosynthetic efficiency and lipid production in freshwater microalga-Scenedesmus obliquus XJ002. Science of the Total Environment 633(3), 593-599.
Jimbo H., Takagi K., Hirashima T., Nishiyama Y., Wada H. 2020. Long-chain saturated fatty acids, palmitic and stearic acids, enhance the repair of photosystem II. International Journal of Molecular Sciences 21(2), 2-9.
Jump D.B. 2002. The biochemistry of n-3 polyunsaturated fatty acids. Journal of Biological Chemistry 277(11), 8755- 8758.
Lavajoo F., Taherizadeh M. 2016. Determination of the growth rates of Spirolina and Chaeatoceros algae in urban waste sewage and their capability to deplete nitrate and phosphate content in the sewage. Journal of Applied Sciences & Environmental Management 20(3), 691-699.
Lee J.Y., Yoo C., Jun S.Y., Ahn C.Y., Oh H.M. 2010. Comparison of several methods for effective lipid extraction from microalgae. Bioresource Technology 101(1), 75-77.
Li Y., Horsman M., Wang B., Wu N., Lan C. 2008. Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Journal of Microbiology and Biotechnology 81(4), 629-636.
Liang Y., Beardall J., Heraud P. 2006. Effects of nitrogen source and UV radiation on the growth, chlorophyll fluorescence and fatty acid composition of Phaeodactylum tricornutum and Chaetoceros muelleri (Bacillariophyceae). Journal of Photochemistry and Photobiology B: Biolog 82(3), 161-172.
Liska A.J., Shevchenko A., Pick U., Katz A. 2004. Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Journal of Plant Physiology 136(1), 2806-2817.
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.
Miquel M., Browse J. 1992. Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis biochemical and genetic characterization of a plant oleoyl- phosphatidylcholine desaturase. The Journal of Biological Chemistry 267(3), 1502-1509.
Narvaez-Zapata J. A., Rojas-Herrera R., Lopez-Uc Y., Sanchez-Estudillo L. 2011. Different physiological responses influenced by salinity in genetically related Dunaliella salina isolates.  Biotechnology Letters 33(5), 1021-1026.
Oren A. 2005. A hundred years of Dunaliella research: 1905-2005. Saline Systems 11, 2.
Pandit P.R., Fulekar M.H., Karuna M.S.L. 2017. Effect of salinity stress on growth, lipid productivity, fatty acid composition, and biodiesel properties in Acutodesmus obliquus and Chlorella vulgaris. Environmental Science and Pollution Research 24(5), 13437–13451.
Priyadarshani I., Rath, B. 2012. Commercial and industrial applications of micro algae. A review. Journal of Algal Biomass Utilization 3(4), 89-100.
Raja R., Hemaiswarya S., Rengasamy R. 2007. Exploitation of Dunaliella for β-carotene production. Applied Microbiology and Biotechnology 4(3), 517-523.
Reshma R., Devi K.C., Kumar S.D., Santhanam P., Perumal P., Krishnaveni N., Kim M. K. 2021. Enhancement of pigments production in the green microalga Dunaliella salina (PSBDU05) under optimized culture condition. Bioresource Technology Reports 14(4), 100672.
Rezayian M., Niknam V., Faramarzi M.A. 2019. Antioxidative responses of Nostoc ellipsosporum and Nostoc piscinale to salt stress. Journal of Applied Phycology 31(1), 157-169.
Salama E.S., Kim H.C., Abou-Shanab R.A.I., Ji M.K., Oh Y.K., Kim S.H., Jeon B.H. 2013. Biomass, lipid content, and fatty acid composition of freshwater Chlamydomonas mexicana and Scenedesmus obliquus grown under salt stress. Bioprocess and Biosystems Engineering 36(6), 827–833.
Salim S., Shi Z., Vermue M.H., Wijffels R.H. 2013. Effect of growth phase on harvesting characteristics, auto flocculation and lipid content of Ettlia texensis for microalgal biodiesel production. Bioresource Technology 138(1), 214-221.
Sanchez-Saavedra M.P., Voltolina D. 2002. Effect of photon fluence rates of white and blue-green light on growth efficiency and pigment content of three diatom species in batch culture. Ciencias Marinas 28(3), 273-279.
Sharma K., Li Y., Schenk P.M. 2014. UV-C-mediated lipid induction and settling, a step change towards economical microalgal biodiesel production. Green Chemistry Journal 16(7), 3539-3548.
Sharma N., Fleurent G., Awwad F., Cheng M., Meddeb-Mouelh F., Budge S.M., Germain H., Desgagne-Penix I. 2020. Red light variation an effective alternative to regulate biomass and lipid profiles in Phaeodactylum tricornutum. Applied Sciences 10(7), 25-31.
Singh R., Upadhyay A.K., Chandra P., Singh D.P. 2018. Sodium chloride incites reactive oxygen species in green algae Chlorococcum humicola and Chlorella vulgaris: implication on lipid synthesis, mineral nutrients, and antioxidant system. Bioresource Technology Journal 270(2), 489-497.
Soufiane Fal. A.B., Abderahim A., Reda Rabie A.C., Abelaziz Smouni B., Hicham E.L., Arroussi A. (2022). Salt induced oxidative stress alters physiological, biochemical and metabolomic responses of green microalga Chlamydomonas reinhardtii. Heliyon Journal 8(1), 1-11.
Sukenik A., Zmora O., Carmeli Y. 1993. Biochemical quality of marine unicellular algae with special emphasis on lipid composition. ll. Nannochloropsis sp. Aquaculture 117(3-4), 313-326.
Takagi M., Karseno, Yoshida T. 2006. Effect of salt concentration on intracellular accumulation of lipidsand triacylglycerides in marine microalgae Dunaliella cells. Bioscience and Bioeneginering 101(3), 223-226.
Teh K.Y., Loh S.H., Aziz A., Takahashi K., Effendy A.W.M., Cha T.S. 2021. Lipid accumulation patterns and role of different fatty acid types towards mitigating salinity fluctuations in Chlorella vulgaris. Scientific Reports. 11(1), 1–12.
Thanapa A., Yolani S., Hitoshi I., Thanit P., Sophon S., Hakuto K., Rungaroon W.S. 2019. Enhanced Lipid Production and Molecular Dynamics under Salinity Stress in Green Microalga Chlamydomonas reinhardtii (137C). Marine Drugs Journal 17(8), 484-499.
Thurakit T., Pumas C., Pathom-aree W., Pekkoh J., Peerapornpisal Y. 2018.  Enhancement of Biomass, Lipid and Hydrocarbon Production from Green Microalga, Botryococcus braunii AARL G037, by UV-C Induction, Chiang Mai Journal of Science 45 (7), 2637-2651.
Tran D., Doan N., Louime C., Giordano M., Portilla S. 2014. Growth, antioxidant capacity and total carotene of Dunaliella salina DCCBC15 in a low cost enriched natural seawater medium. World Journal of Microbiology and Biotechnology 30(1), 317-322.
Wan Afifudeen, C.L., Loh, S.H., Aziz, A., Takahashi, K., Effendy, A.W.M., Cha, T.S. 2021. Double-high in palmitic and oleic acids accumulation in a non-model green microalga, Messastrum gracile SE-MC4 under nitrate-repletion and -starvation cultivations. Scientific Reports 11(2), 1-14.
Wang N., Qian Z., Luo M., Fan S., Zhang X., Zhang L. 2018. Identification of salt stress responding genes using transcriptome analysis in green alga Chlamydomonas reinhardtii. International Journal of Molecular Sciences 19(11), 1-16.
Aquaculture Sciences
Volume 11, Issue 1
March 2023
Pages 72-84

Files

Share

How to cite

Statistics