Abstract
This work aimed to characterize two native microalgal strains newly isolated from South Mediterranean areas and identified as Chlorella sorokiniana ES3 and Neochloris sp. AM2. The growth properties and biochemical composition of these microalgae were evaluated in different culture media (Algal, BG-11, f/2, and Conway). Among the tested media, nitrate- and phosphate-rich Algal medium provided the maximum biomass productivities (85.5 and 111.5 mg l−1 day−1 for C. sorokiniana and Neochloris sp., respectively), while the nitrate- and phosphate-deficient f/2 medium resulted in the highest lipid productivities (24.1 and 35.8 mg l−1 day−1 for C. sorokiniana and Neochloris sp., respectively). The physiological state of both microalgae was investigated under different light and temperature levels using the pulse amplitude-modulated fluorometry. The better photosynthetic efficiency of C. sorokiniana was obtained at 23 °C with a light saturation of 156 μE m−2 s−1, while that of Neochloris sp. was achieved at 15 °C with a light saturation of 151 μE m−2 s−1. The analysis of fatty acid profile and biodiesel parameters revealed that C. sorokiniana, cultivated in Algal and f/2 media, can be considered as a suitable candidate for high-quality biodiesel production.
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Kirrolia, A., Bishnoi, N. R., & Singh, R. (2013). Microalgae as a boon for sustainable energy production and its future research and development aspects. Renewable and Sustainable Energy Reviews, 20, 642–656.
Jazzar, S., Olivares-Carrillo, P., Pérez de los Ríos, A., Marzouki, M. N., Acién-Fernández, F. G., Fernández-Sevilla, J. M., Molina-Grima, E., Smaali, I., & Quesada-Medina, J. (2015). Direct supercritical methanolysis of wet and dry unwashed marine microalgae (Nannochloropsis gaditana) to biodiesel. Applied Energy, 148, 210–219.
Li, L., Cui, J., Liu, Q., Ding, Y., & Liu, J. (2015). Screening and phylogenetic analysis of lipid-rich microalgae. Algal Research, 11, 381–386.
Gao, Y., Yang, M., & Wang, C. (2013). Nutrient deprivation enhances lipid content in marine microalgae. Bioresource Technology, 147, 484–491.
Chaichalerm, S., Pokethitiyook, P., Yuan, W., Meetam, M., Sritong, K., Pugkaew, W., Kungvansaichol, K., Kruatrachue, M., & Damrongphol, P. (2012). Culture of microalgal strains isolated from natural habitats in Thailand in various enriched media. Applied Energy, 89, 296–302.
Zhou, W., Li, Y., Min, M., Hu, B., Chen, P., & Ruan, R. (2011). Local bioprospecting for high-lipid producing microalgal strains to be grown on concentrated municipal wastewater for biofuel production. Bioresource Technology, 102, 6909–6919.
Jazzar, S., Quesada-Medina, J., Olivares-Carrillo, P., Marzouki, M. N., Acién-Fernández, F. G., Fernández-Sevilla, J. M., Molina-Grima, E., & Smaali, I. (2015). A whole biodiesel conversion process combining isolation, cultivation and in situ supercritical methanol transesterification of native microalgae. Bioresource Technology, 190, 281–288.
Álvarez-Díaz, P. D., Ruiz, J., Arbib, Z., Barragán, J., Garrido-Pérez, C., & Perales, J. A. (2014). Lipid production of microalga Ankistrodesmus falcatus increased by nutrient and light starvation in a two-stage cultivation process. Applied Biochemistry and Biotechnology, 174, 1471–1483.
Bertozzini, E., Galluzzi, L., Ricci, F., Penna, A., & Magnani, M. (2013). Neutral lipid content and biomass production in Skeletonema marinoi (Bacillariophyceae) culture in response to nitrate limitation. Applied Biochemistry and Biotechnology, 170, 1624–1636.
Kamalanathan, M., Gleadow, R., & Beardall, J. (2015). Impacts of phosphorus availability on lipid production by Chlamydomonas reinhardtii. Algal Research, 12, 191–196.
Bona, F., Capuzzo, A., Franchino, M., & Maffei, M. E. (2014). Semicontinuous nitrogen limitation as convenient operation strategy to maximize fatty acid production in Neochloris oleoabundans. Algal Research, 5, 1–6.
San Pedro, A., González-López, C. V., Acién, F. G., & Molina-Grima, E. (2015). Outdoor pilot production of Nannochloropsis gaditana: influence of culture parameters and lipid production rates in raceway ponds. Algal Research, 8, 205–213.
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.
Beardall, J., Roberts, S., & Raven, J. A. (2005). Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii. Canadian Journal of Botany, 83, 859–864.
Chu, F. F., Chu, P. N., Shen, X. F., Lam, P. K. S., & Zeng, R. J. (2014). Effect of phosphorus on biodiesel production from Scenedesmus obliquus under nitrogen-deficiency stress. Bioresource Technology, 152, 241–246.
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, 5494–5500.
Arbib, Z., Ruiz, J., Perales, J. A., De Excelencia, C., & Real, P. (2013). Photobiotreatment: influence of nitrogen and phosphorus ratio in wastewater on growth kinetics of Scenedesmus obliquus. International Journal of Phytoremediation, 15, 774–788.
Garrido, M., Cecchi, P., Vaquer, A., & Pasqualini, V. (2013). Effects of sample conservation on assessments of the photosynthetic efficiency of phytoplankton using PAM fluorometry. Deep-Sea Research I, 71, 38–48.
Armi, Z., Trabelsi, E., Turki, S., Ben Maiz, N., & Mahmoudi, E. (2012). Composition and dynamics of potentially toxic dinoflagellates in a shallow Mediterranean lagoon. International Journal of Oceanography and Hydrobiology, 41, 25–35.
Walne, P. R. (1966). Experiments in the large-scale culture of the larvae of Ostrea edulis L. Fishery Investigations Series, 2(25), 1–53.
de la Vega, M., Díaz, E., Vila, M., & León, R. (2011). Isolation of a new strain of Picochlorum sp and characterization of its potential biotechnological applications. Biotechnology Progress, 27, 1535–1543.
Grzebyk, D., Sako, Y., & Berland, B. (1998). Phylogenetic analysis of nine species of Prorocentrum (Dinophyceae) inferred from 18S ribosomal DNA sequences, morphological comparisons, and description of Prorocentrum panamensis, sp. nov. Journal of Phycology, 34, 1055–1068.
Sogin, M. L. (1990). Amplification of ribosomal RNA genes for molecular evolution studies. PCR Protocols: A Guide to Methods and Applications, 307–314.
San Pedro, A., González-López, C. V., Acién, F. G., & Molina-Grima, E. (2013). Marine microalgae selection and culture conditions optimization for biodiesel production. Bioresource Technology, 134, 353–361.
Stanier, R. Y., Kunisawa, R., Mandel, M., & Cohen-Bazire, G. (1971). Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews, 35, 171–205.
Guillard, R. R. L., & Ryther, J. H. (1962). Studies of marine planktonic diatoms: i. Cyclotella nana hustedt, and Detonula confervacea (cleve) gran. Canadian Journal of Microbiology, 8, 229–239.
Ralph, P. J., & Gademann, R. (2005). Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany, 82(3), 222–237.
Jassby, A. D., & Platt, T. (1976). Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography, 21(4), 540–547.
Kochert, G. (1978). Carbohydrate determination by the phenol-sulfuric acid method. In J. S. Hellebust & J. A. Craigie (Eds.), Handbook of physiological and biochemical methods (pp. 96–97). Cambridge: Cambridge Univ. Press.
Dubois, M., Gilles, K., & Hamilton, J. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28(3), 350–356.
AOAC. (1995). Official Methods of Analysis of AOAC International. Washington DC: Association of Official Analytical Chemists.
Doan, T. T. Y., Sivaloganathan, B., & Obbard, J. P. (2011). Screening of marine microalgae for biodiesel feedstock. Biomass and Bioenergy, 35, 2534–2544.
Messaoud, C., Laabidi, A., & Boussaid, M. (2012). Myrtus communis L. infusions: the effect of infusion time on phytochemical composition, antioxidant, and antimicrobial activities. Journal of Food Science, 77, 941–947.
Ramos, M. J., Fernández, C. M., Casas, A., Rodríguez, L., & Pérez, A. (2009). Influence of fatty acid composition of raw materials on biodiesel properties. Bioresource Technology, 100, 261–268.
Kumar, V., Muthuraj, M., Palabhanvi, B., Ghoshal, A. K., & Das, D. (2014). High cell density lipid rich cultivation of a novel microalgal isolate Chlorella sorokiniana FC6 IITG in a single-stage fed-batch mode under mixotrophic condition. Bioresource Technology, 170, 115–124.
Sun, X., Cao, Y., Xu, H., Liu, Y., Sun, J., Qiao, D., & Cao, Y. (2014). Effect of nitrogen-starvation, light intensity and iron on triacylglyceride/carbohydrate production and fatty acid profile of Neochloris oleoabundans HK-129 by a two-stage process. Bioresource Technology, 155, 204–212.
Xia, L., Song, S., He, Q., Yang, H., & Hu, C. (2014). Selection of microalgae for biodiesel production in a scalable outdoor photobioreactor in north China. Bioresource Technology, 174, 274–280.
Aravantinou, A. F., Theodorakopoulos, M. A., & Manariotis, I. D. (2013). Selection of microalgae for wastewater treatment and potential lipids production. Bioresource Technology, 147, 130–134.
Go, S., Lee, S. J., Jeong, G. T., & Kim, S. K. (2012). Factors affecting the growth and the oil accumulation of marine microalgae, Tetraselmis suecica. Bioprocess and Biosystems Engineering, 35, 145–150.
Redfield, A. C. (1958). The biological control of chemical factors in the environment. American Scientist, 46, 205–221.
Carvalho, A. P., Pontes, I., Gaspar, H., & Malcata, F. X. (2006). Metabolic relationships between macro- and micronutrients, and the eicosapentaenoic acid and docosahexaenoic acid contents of Pavlova lutheri. Enzyme and Microbial Technology, 38, 358–366.
Camacho-Rodríguez, J., Cerón-García, M. C., Fernández-Sevilla, J. M., & Molina-Grima, E. (2015). Genetic algorithm for the medium optimization of the microalga Nannochloropsis gaditana cultured to aquaculture. Bioresource Technology, 177, 102–109.
Schreiber, U., & Klughammer, C. (2012). Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynthesis Research, 113, 127–144.
Kobayashi, N., Noel, E. A., Barnes, A., Watson, A., Rosenberg, J. N., Erickson, G., & Oyler, G. A. (2013). Characterization of three Chlorella sorokiniana strains in anaerobic digested effluent from cattle manure. Bioresource Technology, 150, 377–386.
Gatenby, C. M., Orcutt, D. M., Kreeger, D. A., Parker, B. C., Jones, V. A., & Neves, R. J. (2003). Biochemical composition of three algal species proposed as food for captive freshwater mussels. Journal of Applied Phycology, 15, 1–11.
Chisti, Y. (2007). Biodiesel from microalgae. Biotechnology Advances, 25, 294–306.
Liang, K., Zhang, Q., Gu, M., & Cong, W. (2013). Effect of phosphorus on lipid accumulation in freshwater microalga Chlorella sp. Journal of Applied Phycology, 25, 311–318.
Chandra, T. S., Deepak, R. S., Maneesh, M., Mukherji, S., Chauhan, V. S., Sarada, R., & Mudliar, S. N. (2016). Evaluation of indigenous fresh water microalga Scenedesmus obtusus for feed and fuel applications: effect of carbon dioxide, light and nutrient sources on growth and biochemical characteristics. Bioresource Technology, 207, 430–439.
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, 48, 1146–1151.
Ho, S. H., Ye, X., Hasunuma, T., Chang, J. S., & Kondo, A. (2014). Perspectives on engineering strategies for improving biofuel production from microalgae—a critical review. Biotechnology Advances, 32, 1448–1459.
Michelon, W., Da Silva, M. L. B., Mezzari, M. P., Pirolli, M., Prandini, J. M., Soares, H. M. (2015). Effects of nitrogen and phosphorus on biochemical composition of microalgae polyculture harvested from phycoremediation of piggery wastewater digestate. Applied Biochemistry and Biotechnology, 1–13.
Li, T., Zheng, Y., Yu, L., & Chen, S. (2013). High productivity cultivation of a heat-resistant microalga Chlorella sorokiniana for biofuel production. Bioresource Technology, 131, 60–67.
Nascimento, I. A., Cabanelas, I. T. D., dos Santos, J. N., Nascimento, M. A., Sousa, L., & Sansone, G. (2015). Biodiesel yields and fuel quality as criteria for algal-feedstock selection: effects of CO2-supplementation and nutrient levels in cultures. Algal Research, 8, 53–60.
Zheng, Y., Li, T., Yu, X., Bates, P. D., Dong, T., & Chen, S. (2013). High-density fed-batch culture of a thermotolerant microalga Chlorella sorokiniana for biofuel production. Applied Energy, 108, 281–287.
Nascimento, I. A., Marques, S. S. I., Cabanelas, I. T. D., Carvalho, G. C., Nascimento, M. A., Souza, C. O., Druzian, J. I., Hussain, J., & Liao, W. (2014). Microalgae versus land crops as feedstock for biodiesel: productivity, quality, and standard compliance. Bioenergy Research, 7, 1002–1013.
Griffiths, M. J., Van Hille, R. P., & Harrison, S. T. L. (2012). Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. Journal of Applied Phycology, 24, 989–1001.
Francisco, É. C., Neves, D. B., Jacob-Lopes, E., & Franco, T. T. (2010). Microalgae as feedstock for biodiesel production: carbon dioxide sequestration, lipid production and biofuel quality. Journal of Chemical Technology and Biotechnology, 85, 395–403.
Acknowledgments
The authors gratefully acknowledge the Tunisian Ministry of Higher Education and Scientific Research-University of Carthage (Tunisia) for supporting Souhir Jazzar with a grant for young researcher for a period of 3 years during her thesis. The authors would like to acknowledge the professors, Emilio Molina-Grima, Francisco Gabriel Acién-Fernández, and José María Fernández-Sevilla from the Department of Chemical Engineering, University of Almería, E-04120 Almería (Spain), for their relevant discussions and scientific support in the PAM measurements of microalgae. The authors are also grateful to Ms. Donia Weslati for the English check of the manuscript.
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Jazzar, S., Berrejeb, N., Messaoud, C. et al. Growth Parameters, Photosynthetic Performance, and Biochemical Characterization of Newly Isolated Green Microalgae in Response to Culture Condition Variations. Appl Biochem Biotechnol 179, 1290–1308 (2016). https://doi.org/10.1007/s12010-016-2066-z
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DOI: https://doi.org/10.1007/s12010-016-2066-z