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Influence of salinity, nitrogen and phosphorus concentrations on the physiological and biochemical characteristics of two Chlorophyceae isolated from Fez freshwater, Morocco – Scientific Reports

  • Bajpai, P. Fuel potential of third generation biofuels. In Third Generation Biofuels (ed. Bajpai, P.) 7–10 (Springer, 2019). https://doi.org/10.1007/978-981-13-2378-2_2.

    Chapter 

    Google Scholar
     

  • Ganesan, R. et al. A review on prospective production of biofuel from microalgae. Biotechnol. Rep. 27, e00509 (2020).

    Article 

    Google Scholar
     

  • Mutanda, T. et al. Bioprospecting for hyper-lipid producing microalgal strains for sustainable biofuel production. Bioresour. Technol. 102, 57–70 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Markou, G. & Nerantzis, E. Microalgae for high-value compounds and biofuels production: A review with focus on cultivation under stress conditions. Biotechnol. Adv. 31, 1532–1542 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Magierek, E. & Krzemińska, I. Effect of stress conditions on improvement of lipid and carbohydrate accumulation under photoautotrophic cultivation of Chlorophyta. Phycologia 57, 601–618 (2018).

    Article 

    Google Scholar
     

  • Jazzar, S., Berrejeb, N., Messaoud, C., Marzouki, M. N. & Smaali, I. 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).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krichen, E., Rapaport, A., Le Floc’h, E. & Fouilland, E. Demonstration of facilitation between microalgae to face environmental stress. Sci. Rep. 9, 16076 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Briddon, C. L. et al. The combined impact of low temperatures and shifting phosphorus availability on the competitive ability of cyanobacteria. Sci. Rep. 12, 16409 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bibi, F., Jamal, A., Huang, Z., Urynowicz, M. & Ishtiaq Ali, M. Advancement and role of abiotic stresses in microalgae biorefinery with a focus on lipid production. Fuel 316, 123192 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Chu, F.-F. et al. Phosphorus plays an important role in enhancing biodiesel productivity of Chlorella vulgaris under nitrogen deficiency. Bioresour. Technol. 134, 341–346 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yaakob, M. A., Mohamed, R. M. S. R., Al-Gheethi, A., Aswathnarayana Gokare, R. & Ambati, R. R. Influence of nitrogen and phosphorus on microalgal growth, biomass, lipid, and fatty acid production: An overview. Cells 10, 393 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pandit, P. R., Fulekar, M. H. & Karuna, M. S. L. Effect of salinity stress on growth, lipid productivity, fatty acid composition, and biodiesel properties in Acutodesmus obliquus and Chlorella vulgaris. Environ. Sci. Pollut. Res. 24, 13437–13451 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Hassi, M., Mohamed, A., Ouaddi, O. & Oukarroum, A. A review of Moroccan microalgae and their exploitation fields. IOSR 14(7), 53–59. https://doi.org/10.9790/2402-1407015359 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Maadane, A. et al. Antioxidant activity of some Moroccan marine microalgae: Pufa profiles, carotenoids and phenolic content. J. Biotechnol. 215, 13–19 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • El Arroussi, H. et al. Screening of marine microalgae strains from Moroccan coasts for biodiesel production. Renew. Energy 113, 1515–1522 (2017).

    Article 

    Google Scholar
     

  • Idrissi, A. A., Mohamed, B., Mohammed, A. M. & Lotfi, A. Growth performance and biochemical composition of nineteen microalgae collected from different Moroccan reservoirs. Mediterr. Mar. Sci. 17, 323 (2016).

    Article 

    Google Scholar
     

  • Youssef, M., Brakez, Z., Yassine, E. & Lhoucine, B. Investigation of lipid production and fatty acid composition in some native microalgae from Agadir region in Morocco. Afr. J. Biotechnol. 19, 754–762 (2020).

    Article 

    Google Scholar
     

  • Shetty, P., Gitau, M. & Maróti, G. Salinity stress responses and adaptation mechanisms in eukaryotic green microalgae. Cells 8, 1657 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, L. et al. Salinity-induced cellular cross-talk in carbon partitioning reveals starch-to-lipid biosynthesis switching in low-starch freshwater algae. Bioresour. Technol. 250, 449–456 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Talebi, A. F., Tabatabaei, M., Mohtashami, S. K., Tohidfar, M. & Moradi, F. Comparative salt stress study on intracellular ion concentration in marine and salt-adapted freshwater strains of microalgae. Not. Sci. Biol. 5, 309–315 (2013).

    Article 
    CAS 

    Google Scholar
     

  • El-Sheekh, M. M., Galal, H. R., Mousa, A. S. H. & Farghl, A. A. M. Impact of macronutrients and salinity stress on biomass and biochemical constituents in Monoraphidium braunii to enhance biodiesel production. Sci. Rep. 14, 2725 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bartolomé, M. C., D’ors, A. & Sánchez-Fortún, S. Toxic effects induced by salt stress on selected freshwater prokaryotic and eukaryotic microalgal species. Ecotoxicology 18, 174–179 (2009).

    Article 
    PubMed 

    Google Scholar
     

  • Li, S. et al. Mechanism study on the regulation of metabolite flux for producing promising bioactive substances in microalgae Desmodesmus sp. YT through salinity stress. Algal Res. 64, 102721 (2022).

    Article 

    Google Scholar
     

  • Ji, X. et al. The effect of NaCl stress on photosynthetic efficiency and lipid production in freshwater microalga—Scenedesmus obliquus XJ002. Sci. Total Environ. 633, 593–599 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Sedjati, S. et al. Chlorophyll and carotenoid content of Dunaliella salina at various salinity stress and harvesting time. IOP Conf. Ser. Earth Environ. Sci. 246, 012025 (2019).

    Article 

    Google Scholar
     

  • Sun, X.-M. et al. Influence of oxygen on the biosynthesis of polyunsaturated fatty acids in microalgae. Bioresour. Technol. 250, 868–876 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, H. & Wang, Q. Regulatory mechanisms of lipid biosynthesis in microalgae. Biol. Rev. Camb. Philos. Soc. 96, 2373–2391 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hamed, S. M., Selim, S., Klöck, G. & AbdElgawad, H. Sensitivity of two green microalgae to copper stress: Growth, oxidative and antioxidants analyses. Ecotoxicol. Environ. Saf. 144, 19–25 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yun, C.-J., Hwang, K.-O., Han, S.-S. & Ri, H.-G. The effect of salinity stress on the biofuel production potential of freshwater microalgae Chlorella vulgaris YH703. Biomass Bioenergy 127, 105277 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Pancha, I. et al. Nitrogen stress triggered biochemical and morphological changes in the microalgae Scenedesmus sp. CCNM 1077. Bioresour. Technol. 156, 146–154 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • von Alvensleben, N., Magnusson, M. & Heimann, K. Salinity tolerance of four freshwater microalgal species and the effects of salinity and nutrient limitation on biochemical profiles. J. Appl. Phycol. 28, 861–876 (2016).

    Article 

    Google Scholar
     

  • Grobbelaar, J. Algal nutrition: Mineral nutrition. In Handbook of Microalgal Culture: Biotechnology and Applied Phycology (ed. Richmond, A.) 95–115 (Blackwell Publishing, 2007). https://doi.org/10.1002/9780470995280.ch6.

    Chapter 

    Google Scholar
     

  • Markou, G., Vandamme, D. & Muylaert, K. Microalgal and cyanobacterial cultivation: The supply of nutrients. Water Res. 65, 186–202 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, T. et al. Biochemical and morphological changes triggered by nitrogen stress in the oleaginous microalga Chlorella vulgaris. Microorganisms 10, 566 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, T. et al. Morphology, growth, biochemical composition and photosynthetic performance of Chlorella vulgaris (Trebouxiophyceae) under low and high nitrogen supplies. Algal Res. 16, 481–491 (2016).

    Article 

    Google Scholar
     

  • da Silva Ferreira, V. & Sant’Anna, C. Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World J. Microbiol. Biotechnol. 33, 20 (2017).

    Article 
    PubMed 

    Google Scholar
     

  • Li, L., Zhang, L. & Liu, J. Proteomic analysis of hydrogen production in Chlorella pyrenoidosa under nitrogen deprivation. Algal Res. 53, 102143 (2021).

    Article 

    Google Scholar
     

  • Rai, V., Muthuraj, M., Gandhi, M. N., Das, D. & Srivastava, S. Real-time iTRAQ-based proteome profiling revealed the central metabolism involved in nitrogen starvation induced lipid accumulation in microalgae. Sci. Rep. 7, 45732 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fatini, M. A., Basri, E. M. & Maznah, W. O. W. Effect of different nitrogen sources on cell growth and biochemical compositions of Chlorococcum sp. cultivated under laboratory conditions. IOP Conf. Ser. Earth Environ. Sci. 711, 012010 (2021).

    Article 

    Google Scholar
     

  • Solovchenko, A. et al. Phosphorus starvation and luxury uptake in green microalgae revisited. Algal Res. 43, 101651 (2019).

    Article 

    Google Scholar
     

  • Liang, M.-H., Qv, X.-Y., Chen, H., Wang, Q. & Jiang, J.-G. Effects of salt concentrations and nitrogen and phosphorus starvations on neutral lipid contents in the green microalga Dunaliella tertiolecta. J. Agric. Food Chem. 65, 3190–3197 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Procházková, G., Brányiková, I., Zachleder, V. & Brányik, T. Effect of nutrient supply status on biomass composition of eukaryotic green microalgae. J. Appl. Phycol. 26, 1359–1377 (2014).

    Article 

    Google Scholar
     

  • Solovchenko, A. E. et al. Luxury phosphorus uptake in microalgae. J. Appl. Phycol. 31, 2755–2770 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Maltsev, Y., Kulikovskiy, M. & Maltseva, S. Nitrogen and phosphorus stress as a tool to induce lipid production in microalgae. Microb. Cell Factories 22, 239 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Thrane, J.-E., Hessen, D. O. & Andersen, T. Plasticity in algal stoichiometry: Experimental evidence of a temperature-induced shift in optimal supply N:P ratio. Limnol. Oceanogr. 62, 1346–1354 (2017).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Xin, L., Hong-ying, H., Ke, G. & Ying-xue, S. Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresour. Technol. 101, 5494–5500 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rai, M. P., Gautom, T. & Sharma, N. Effect of salinity, pH, light intensity on growth and lipid production of microalgae for bioenergy application. OnLine J. Biol. Sci. 15, 260–267 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Guimarães, B. S. & França, K. B. Statistical study of growth kinetics and lipid content of microalgae grown in brackish waters for bioenergetic purposes. Rev. Ambiente Água 16, e2649 (2021).

    Article 

    Google Scholar
     

  • Kirrolia, A., Bishnoi, N. & Singh, R. Effect of shaking, incubation temperature, salinity and media composition on growth traits of green microalgae Chlorococcum sp.. J. Algal Biomass Util. 3, 46–53 (2012).


    Google Scholar
     

  • Teh, K. Y. et al. Lipid accumulation patterns and role of different fatty acid types towards mitigating salinity fluctuations in Chlorella vulgaris. Sci. Rep. 11, 438 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chiu, L., Ho, S.-H., Shimada, R., Ren, N.-Q. & Ozawa, T. Rapid in vivo lipid/carbohydrate quantification of single microalgal cell by Raman spectral imaging to reveal salinity-induced starch-to-lipid shift. Biotechnol. Biofuels 10, 9 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klok, A. J., Lamers, P. P., Martens, D. E., Draaisma, R. B. & Wijffels, R. H. Edible oils from microalgae: Insights in TAG accumulation. Trends Biotechnol. 32, 521–528 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ho, S.-H. et al. Dynamic metabolic profiling together with transcription analysis reveals salinity-induced starch-to-lipid biosynthesis in alga Chlamydomonas sp. JSC4. Sci. Rep. 7, 45471 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Singh, P., Guldhe, A., Kumari, S., Rawat, I. & Bux, F. Investigation of combined effect of nitrogen, phosphorus and iron on lipid productivity of microalgae Ankistrodesmus falcatus KJ671624 using response surface methodology. Biochem. Eng. J. 94, 22–29 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Wehr, J. D., Sheath, R. G. & Kociolek, J. P. Freshwater Algae of North America: Ecology and Classification (Elsevier, 2015).


    Google Scholar
     

  • Singh, R., Upadhyay, A. K., Chandra, P. & Singh, D. P. Sodium chloride incites reactive oxygen species in green algae Chlorococcum humicola and Chlorella vulgaris: Implication on lipid synthesis, mineral nutrients and antioxidant system. Bioresour. Technol. 270, 489–497 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chng, L. M., Lee, K. T. & Chan, D. C. J. Evaluation on microalgae biomass for bioethanol production. IOP Conf. Ser. Mater. Sci. Eng. 206, 012018 (2017).

    Article 

    Google Scholar
     

  • Jeffrey, S. W., Mantoura, R. F. C. & Wright, S. W. Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods 181–223 (UNESCO Publishing, 1997).


    Google Scholar
     

  • Folch, J., Lees, M. & Sloane Stanley, G. H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497–509 (1957).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Amenta, J. A rapid method for quantification of lipids separated by thin-layer chromatopraphy. J. Lipid Res. 5, 270–272 (1964).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Alaoui, M. M. Dynamique des populations et évolution métabolique du phytoplancton dans un lac eutrophe (Lac Aydat, PUY de DOME, France). Université Blaise Pascal (Clermont-Ferrand II) U.F.R. de la Recherche Scientifique et Technique. Imp Sciences 63177 Aubiere CEDEX (1985).

  • Bates, L. S., Waldren, R. P. & Teare, I. D. Rapid determination of free proline for water-stress studies. Plant Soil 39, 205–207 (1973).

    Article 
    CAS 

    Google Scholar
     

  • Velikova, V., Yordanov, I. & Edreva, A. Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci. 151, 59–66 (2000).

    Article 
    CAS 

    Google Scholar