Characterization of a new Dunalliela salina strain isolated from San Quintin, Baja California (México) producer of lipids, pigments and micronutrients
DOI:
https://doi.org/10.37543/oceanides.v33i2.212Keywords:
Dunaliella salina, green microalgae, pigments, sea salt fields, salinity challengeAbstract
Some microalgae are recognized for producing pigments and other metabolites with biotechnological importance, particularly, Dunaliella salina is a remarkable one. These kind of compounds are used as food and have a great industrial potential. The pigment industry comprises a millionaire market value, being β-carotene one of the most profitable one. In this study we describe the morphology, molecular identification, growth dynamics, proximal composition, nutrients and pigment content of a recently isolated Dunaliella salina strain (SQ) under different salinity/light conditions, in order to highlight its remarkable properties for biotech/biomed industry. D. salina SQ reached the highest densities (1.07-1.25 cell mL-1 x106) at low salinities (100-500 mM NaCl) under continuous light regimen (24:0 h Light:Dark). Neoxanthin (Neo) and violaxanthin (Viol) were the most abundant pigments when exposed to 500 mM NaCl (18:6 h Light:Dark). Furthermore, this peculiar strain produces other compounds with high industrial value.
Downloads
References
AOAC, 1990. Official methods of analysis 15th Ed, in Association of official analytical chemists, Washington, DC, USA.
Abomohra, A.E.F., W. Jin, R. Tu, S. F. Han, M. Eid & H. Eladel. 2016. Microalgal biomass production as a sustainable feedstock for biodiesel: Current status and perspectives. Renewable and Sustainable Energy Reviews, 64: 596-606. https://doi.org/10.1016/j.rser.2016.06.056
Almazán-Becerril, A. & E. García-Mendoza. 2008. Maximum efficiency of charge separation of photosystem II of the phytoplankton community in the Eastern Tropical North Pacific off México: A nutrient stress diagnostic tool ? Ciencias Marinas, 34(1): 29-43. https://doi.org/10.7773/cm.v34i1.1151
Andersen, A.R. 2005. Algal Culturing Techniques. (Andersen A. Robert, Ed.). 589 p.
Assunção, P., R. Jaén-Molina, J. Caujapé-Castells, M. Wolf, M. A. Buchheim, A. de la Jara & H. Mendoza. 2013. Phylogenetic analysis of ITS2 sequences suggests the taxonomic re-structuring of Dunaliella viridis (Chlorophyceae, Dunaliellales). Phycological Research, 61(2): 81-88. https://doi.org/10.1111/pre.12003
Barzegari, A., M. A. Hejazi, N. Hosseinzadeh, S. Eslami, E. Mehdizadeh Aghdam & M. S. Hejazi. 2010. Dunaliella as an attractive candidate for molecular farming. Molecular Biology Reports, 37(7): 3427-3430. https://doi.org/10.1007/s11033-009-9933-4
Becker E.W. 2007. Micro-algae as a source of protein. Biotechnology Advances, 25(2): 207-210. https://doi.org/10.1016/j.biotechadv.2006.11.002
Belghith T., K. Athmouni, J. Elloumi, W. Guermazi, T. Stoeck & H. Ayadi. 2015. Biochemical Biomarkers in the Halophilic Nanophytoplankton: Dunaliella salina Isolated from the Saline of Sfax (Tunisia). Arabian Journal for Science and Engineering, 17-24. https://doi.org/10.1007/s13369-015-1808-5
Ben-Amotz, A. 1993. Production of B-Carotene and Vitamins by the Halotolerant Alga Dunaliella. 411-417, In: Marine Biotechnology (Vol. 1). New York. https://doi.org/10.1007/978-1-4899-2391-2_11
Ben-Amotz, A. & M. Avron. 1983. On the Factors Which Determine Massive beta-Carotene Accumulation in the Halotolerant Alga Dunaliella bardawil. Plant Physiology, 72(3): 593-597. https://doi.org/10.1104/pp.72.3.593
Benavente-Valdés, J. R., C. Aguilar, J. C. Contreras-Esquivel, A. Méndez-Zavala & J. Montañez. 2016. Strategies to enhance the production of photosynthetic pigments and lipids in chlorophyceae species. Biotechnology Reports, 10: 117-125. https://doi.org/10.1016/j.btre.2016.04.001
Bligh E. G. & W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and hysiology, 37: 911-917. https://doi.org/10.1139/y59-099
Borowitzka, M. A. 1990. Technical resource papers: The Mass Culture of Dunaliella salina. Retrieved from http://www.fao.org/docrep/ field/003/ab728e/ab728e06.htm
Borowitzka, M. A. 1988. Algal Growth Media and Sources. 456-465, In: Micro-algal Biotechnology. Retrieved from http://www.fao.org/docrep/ field/003/ab728e/ab728e06.htm
Borowitzka, M. A. 2013. High-value products from microalgae-their development and commercialization. Journal of Applied Phycology, 25(3): 743-756. https://doi.org/10.1007/s10811-013-9983-9
Borowitzka, M. A. & C. J. Silva. 2007. The taxonomy of the genus Dunaliella (Chlorophyta, Dunaliellales) with emphasis on the marine and halophilic species. Journal of Applied Phycology, 19(5): 567-590. https://doi.org/10.1007/s10811-007-9171-x
Cade-Menun, B. J. & A. Paytan. 2010. Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Marine Chemistry, 121: 27-36. https://doi.org/10.1016/j.marchem.2010.03.002
Cadoret, J. P., M. Garnier & B. Saint-Jean. 2012. Microalgae, Functional Genomics and Biotechnology. Advances in Botanical Research (Vol. 64).
Cai, M., L.H. He & T.Y. Yu. 2013. Molecular Clone and Expression of a NAD+-Dependent Glycerol-3-Phosphate Dehydrogenase Isozyme Gene from the Halotolerant alga Dunaliella salina. PLoS ONE, 8(4): 1-8. https://doi.org/10.1371/journal.pone.0062287
Chen, Y., T. Xu, R. K. Vijay, C. Xu & S. Vaidyanathan. 2015. Influence of nutrient status on the accumulation of biomass and lipid in Nannochloropsis salina and Dunaliella salina, Energy Conversion and Management. Elsevier Ltd, 106 p. https://doi.org/10.1016/j.enconman.2015.09.025
Dubois, M., K.A. Gilles, J.K. Hamilton, P.A. Rebers & F. Smith. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28: 350-356. https://doi.org/10.1021/ac60111a017
Dufossé, L., P. Galaup, A. Yaron, S. M. Arad, P. Blanc, K. N. C. Murthy & G.A. Ravishankar. 2005. Microorganisms and microalgae as sources of pigments for food use: A scientific oddity or an industrial reality? Trends in Food Science and Technology, 16(9): 389-406. https://doi.org/10.1016/j.tifs.2005.02.006
Farhat, N., M. Rabhi, H. Falleh, J. Jouini, C. Abdelly & A. Smaoui. 2011. Optimization of salt concentrations for a higher carotenoid production in Dunaliella salina (Chlorophyceae). Journal of Phycology, 47(5): 1072-1077. https://doi.org/10.1111/j.1529-8817.2011.01036.x
Fox, J. 2017. Using the R Commander. A Point-and Click Interface for R. CRC Press. CHAPMAN & HALL, USA.
Frank, H. A. & R. J. Cogdell. 1996. Carotenoids in Photosynthesis. Photochemistry and Photobiology. Wiley Online Library. https://doi.org/10.1111/j.1751-1097.1996.tb03022.x
Ganesan, V. S. H. 2014. Biomass from Microalgae: An Overview. Oceanography: Open Access, 2(1): 1-7. https://doi.org/10.4172/2332-2632.1000118
Guevara, M., R. Pinto, J. Villarroel, E. Hernández, R. Díaz & B.R.C. Gotera. 2016. Influencia de la salinidad y la irradiancia sobre el crecimiento y composición bioquímica de una nueva cepa de Dunaliella salina, proveniente de las salinas de Araya, Venezuela. Saber, 28: 494-501.
Goltekar, R.C., K.P. Krishnan, M.J.B.D. De Souza, A.L. Paropkari & P.A. Loka Bharathi. 2006. Effect of carbon source concentration and culture duration on retrievability of bacteria from certain estuarine, coastal and offshore areas around eninsular India. Current Science, 90(1): 103-106.
Gonçalves, A. L., M. Simões & J.C.M. Pires. 2014. The effect of light supply on microalgal growth, CO 2 uptake and nutrient removal from wastewater. Energy Convers Manage, 85: 530-6. https://doi.org/10.1016/j.enconman.2014.05.085
Griffiths, M. J., R. P. van Hille & S.T. Harrison. 2012. Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. Journal of Applyed Phycology, 24: 989-1001. https://doi.org/10.1007/s10811-011-9723-y
Guo-Zhong, J., L. Yu-Min, N. Xiang-Li & X. LeXun. 2005. The actin gene promoter-driven bar as a dominant selectable marker for nuclear transformation of Dunaliella salina. Acta Genetica Sinica, 32(4): 424-433.
Heukelem, L. Van & C. S. Thomas. 2001. Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments, Journal of Chromatography A, 910: 31-49. https://doi.org/10.1016/S0378-4347(00)00603-4
Jackson, M. L. 1973. Soil Chemical Analysis. Prentice-Hall of India Pvt. Ltd., New Delhi, India.
Jayappriyan, K. R., R. Rajkumar, P. R. Kannan, S. Divya & R. Rengasamy. 2010. Significance of 18S rDNA specific primers in the identification of genus Dunaliella, Journal of Experimental Sciences, 1(1): 27-31.
Johnson, M. K., E. J. Johnson, R. D. MacElroy, H. L. Speer & B. S. Bruff. 1968. Effects of salts on the halophilic alga Dunaliella viridis. Journal of Bacteriology, 95(4): 1461-1468. https://doi.org/10.1128/JB.95.4.1461-1468.1968
Kadkhodaei, S., A.B. Ariff & H.R. Memari. 2011. Construction of an expression vector for production of tissue plasminogen activator (t-PA) in a transgenic microalgae bioreactor. International Conference on Biomedical Engineering and Technology, 11: 193-196.
Kotake-Nara, E., M. Kushiro, H. Zhang, T. Sugawara, K. Miyashita & A. Nagao. 2001. Carotenoids affect proliferation of human prostate cancer cells. The Journal of Nutrition, 131(12): 3303-3306. https://doi.org/10.1093/jn/131.12.3303
Lamers, P.P., M. Janssen, R.C.H. De Vos, R.J. Bino & R.H. Wijffels. 2008. Exploring and exploiting carotenoid accumulation in Dunaliella salina for cell-factory applications. Trends in Biotechnology, 26(11): 631-638. https://doi.org/10.1016/j.tibtech.2008.07.002
Loeblich, L. 1982. Photosynthesis and pigments influenced by light intensity and salinity in the halophile Dunaliella salina (Chlorophyta). Journal of the Marine Biological Association of the UK, 62: 493-508. https://doi.org/10.1017/S0025315400019706
Lopez, H., D. Magdaleno & J. Stephano. 2017. The complete chloroplast genome of the green microalgae Dunaliella salina strain SQ. Mitochondrial DNA Part B, 2(1): 225-226. https://doi.org/10.1080/23802359.2017.1310610
Lowry, O. H., H.J. Rosebrough, A.L. Farr & R.J. Randall. 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193: 265-275. https://doi.org/10.1016/S0021-9258(19)52451-6
Lundquist, T.J., I.C. Woertz, N.W.T. Quinn & J.R. Benemann. 2010. A Realistic Technology and Engineering Assessment of Algae Biofuel Production. Energy, (October), 1-14. https://doi.org/10.1556/1848.2015.6.1.6
Magdaleno, D., H. Lopez & J. Stephano 2017. The complete mitochondrial genome of the green microalgae Dunaliella salina strain SQ. Mitochondrial DNA Part B, 2(1): 311-312. https://doi.org/10.1080/23802359.2017.1331331
Niyogi, K.K., O. Bjorkman & A. Grossman R. 1997. The roles of specific xanthophylls in photoprotection. Proceedings of the National Academy of Sciences, 94(25): 14162-14167. https://doi.org/10.1073/pnas.94.25.14162
Olmos-Soto, J., J. Paniagua-Michel, R. Contreras & L. Trujillo. 2002. Molecular identification of β-carotene hyper-producing strains of Dunaliella from saline environments using species-specific oligonucleotides. Biotechnology Letters, 24(5): 365-369. https://doi.org/10.1023/A:1014516920887
Olmos-Soto, J., L. Ochoa, J. Paniagua-Michel & R. Contreras. 2009. DNA fingerprinting differentiation between beta-carotene hyperproducer strains of Dunaliella from around the world. Saline Systems, 5: 5. https://doi.org/10.1186/1746-1448-5-5
Olmos-Soto, J., J. Paniagua & R. Contreras. 2000. Molecular identification of Dunaliella sp. utilizing the 18S rDNA gene. Letters in Applied Microbiology, 30(1): 80-84. https://doi.org/10.1046/j.1472-765x.2000.00672.x
Oren, A. 2005. A hundred years of Dunaliella research: 1905-2005. Saline Systems, 1: 2. https://doi.org/10.1186/1746-1448-1-2
Oren, A. 2010. Industrial and environmental applications of halophilic microorganisms. Environmental Technology, 31: 825-834. https://doi.org/10.1080/09593330903370026
Pancha, I., K. Chokshi, T. Ghosh, C. Paliwal, R. Maurya & S. Mishra. 2015. Bicarbonate supplementation enhanced biofuel production potential as well as nutritional stress mitigation in the microalgae Scenedesmus sp. CCNM 1077. Bioresource Technology, 193: 315-323. https://doi.org/10.1016/j.biortech.2015.06.107
Paniagua-Michel, J., Capa-Robles W., Olmos-Soto J. & Gutierrez-Millan L.E. 2009. The carotenogenesis pathway via the isoprenoid-beta-carotene interference approach in a new strain of Dunaliella salina isolated from Baja California México. Marine Drugs, 7(1): 45-56. https://doi.org/10.3390/md7010045
Pasquet, V., P. Morisset, S. Ihammouine, A. Chepied, L. Aumailley, J. B. Berard, B. Serive, R. Kaas, I. Lanneluc, V. Thiery, M. Lafferriere, J. M. Piot, T. Patrice, J.P. Cadoret & L. Picot. 2011. Antiproliferative activity of violaxanthin isolated from bioguided fractionation of Dunaliella tertiolecta extracts. Marine Drugs, 9(5): 819-831. https://doi.org/10.3390/md9050819
Pisal, D. S. & S.S. Lele. 2005. Carotenoid production from microalga, Dunaliella salina. Indian Journal of Biotechnology, 4(4): 476-483.
Pulz, O. & W. Gross. 2004. Valuable products from biotechnology of microalgae. Applied Microbiology and Biotechnology, 65(6): 635-648. https://doi.org/10.1007/s00253-004-1647-x
Rappé, M.S., S.A. Connon, K.L. Vergin & S.J. Giovannoni. 2002. Cultivation of the ubiquitous SAR 11 marine bacterioplankton clade. Nature, 418: 630-3. https://doi.org/10.1038/nature00917
Reber, L.A. & M.M. Wallace, 1937. Chlorides and Bromides. Analytical Edition, 167(1): 1937.
Richmond, A. & Q. Hu 2013. Handbook of Microalgal Culture: Applied Phycology and Biotechnology, Second Edition. Wiley-Blackwell. ISBN 9780470673898, 9781118567166. 726 p. https://doi.org/10.1002/9781118567166
Sambrook, J., E.F. Fritsch & T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press.
Smith, D.R., R.W. Lee, J.C. Cushman, J.K. Magnuson, D. Tran. & J.E. Polle. 2010. The Dunaliella salina organelle genomes: large sequences, inflated with intronic and intergenic DNA. BMC Plant Biology, 10: 83. https://doi.org/10.1186/1471-2229-10-83
Soontornchaiboon, W., S.S. Joo & S.M. Kim. 2012. Anti-inflammatory Effects of Violaxanthin Isolated from Microalga Chlorella ellipsoidea in RAW 264.7 Macrophages. Biological and Pharmaceutical Bulletin, 35: 1137-1144. https://doi.org/10.1248/bpb.b12-00187
Speight, J.G. 2013. The chemistry and technology of coal. Fuel and Energy Abstracts, 36(3): 835. https://doi.org/10.1016/0140-6701(95)80007-7
Thaipratum, R., A. Melis, J. Svasti & K. Yokthongwattana. 2009. Analysis of non- photochemical energy dissipating processes in wild type Dunaliella salina (green algae) and in zea1, a mutant constitutively accumulating zeaxanthin. Journal of Plant Research, 122: 465-476. https://doi.org/10.1007/s10265-009-0229-5
Tokuşoglu, O. & M.K. üUnal. 2003. Biomass Nutrient Profiles of Three Microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrysis galbana. Journal of Food Science, 68(4): 1144-1148. https://doi.org/10.1111/j.1365-2621.2003.tb09615.x
Walkley, A. & I.A. Black. 1934. An examination of the Degtjareff method for determining organic carbon in soils: Effect of variations in digestion conditions and of inorganic soil constituents. Soil Science, 63:251-263. https://doi.org/10.1097/00010694-194704000-00001
Wen, Z.Y. & F. Chen, 2003. Heterotrophic production of eicosapentaenoic acid by microalgae. Biotechnology Advances, 21(4): 273-294. https://doi.org/10.1016/S0734-9750(03)00051-X
Widowati, W. & A. Asnah. 2014. Biochar effect at potassium fertilizer and dosage leaching potassium for two-corn planting season. AGRIVITA Journal of Agricultural Science, 36(1): 65-71. Retrieved from https://doi.org/10.17503/Agrivita-2014-36-1-p065-071
Wilcox, L.W., L.A. Lewis, P. A. Fuerst & G.L. Floyd. 1992. Group I introns within the nuclear-encoded small-subunit rRNA gene of three green algae. Molecular Biology and Evolution, 9(6): 1103-18. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1435237.
Yaakob, Z., E. Ali, A. Zainal, M. Mohamad. & M. Takriff. 2014. An overview: biomolecules from microalgae for animal feed and aquaculture. Journal of Biological Research-Thessaloniki, 21(1): 6. https://doi.org/10.1186/2241-5793-21-6
Zhang, Z., S. Schwartz, L. Wagner & W. Miller. 2000. A greedy algorithm for a aligning DNA sequences. Journal of Computational Biology, 7(1-2): 203-214. https://doi.org/10.1089/10665270050081478
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2018 Ricardo Valencia, Ivone Giffard-Mena, Ricardo Cruz-López, Ernesto García-Mendoza, José Luis Stephano-Hornedo
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License 4.0 that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.