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Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena gracilis, Chlorella vulgaris) and Marine (Pavlova lutheri, Diacronema vlkanium) Microalgae

Year 2024, Volume: 39 Issue: 1, 8 - 16, 09.01.2024
https://doi.org/10.26650/ASE20241303511

Abstract

This work is focused on investigating the nutrient compositions, growth, and fatty acid composition of Chlorella vulgaris, Euglena gracilis, Pavlova lutheri, and Diacronema vlkanium, which are natural diets of bivalve, crustaceans, live prey such as rotifer, copepods, daphnia and feed ingredients in aquaculture nutrition. Microalgae culture was performed in a live feed laboratory under controlled physical and chemical conditions. The initial concentration of microalgae species was adjusted as 2×106 cells/mL and growth performance was calculated by Neubauer Hemocytometer daily. The maximum growth performance was detected in Diacronema vlkanium culture with 1.78×107 cells/mL. In the case of proximate composition, the highest dry matter content was found in Pavlova lutheri (6.21%). Freshwater microalgae species Chlorella vulgaris (50.5%) and Euglena gracilis (42.5%) had high crude protein compared to Pavlova lutheri and Diacronema vlkanium. Fatty acid compositions of microalgae were also determined. The highest EPA (C20:5n-3) content was found in Pavlova lutheri (6.85%) whereas arachidonic acid (C20:4n-6) and docosahexaenoic acid (C22:6n-3) contents were only found with a level of (3.32%) and (1.79%) in Euglena gracilis, respectively. Microalgal culture should have high biomass in a short time of culture and in this study, E.gracilis and P.lutheri showed high growth and essential nutrients gain in laboratory scale production and this result could be applied in larger volume photobioreactor.

Supporting Institution

Istanbul University, Scientific Research Foundation

Project Number

FLO-2022-39273

References

  • AOAC (1995). Official methods of analysis of the association of analytical chemistry (15th ed.). Arlington, VA: AOAC. google scholar
  • Ahmed, F., Zhou, W., & Schenk, P. M. (2015). Pavlova lutheri is a high-level producer of phytosterols. Algal Research, 10, 210-217. https://doi. org/10.1016/j.algal.2015.05.013 google scholar
  • Ahmad, M. T., Shariff, M., Md. Yusoff, F., Goh, Y. M., & Banerjee, S. (2020). Applications of microalga Chlorella vulgaris in aquaculture. Reviews in Aquaculture, 12(1), 328-346. https://doi.org/10.1111/raq.12320 google scholar
  • Arkronrat, W., Deemark, P., & Oniam, V. (2016). Growth performance and proximate composition of mixed cultures of marine microalgae (Nannochloropsis sp.& Tetraselmis sp.)withmonocultures. Songklanakarin Journal of Science and Technology, 38(1), 1-5. google scholar
  • Aslam, A., Rasul, S., Bahadar, A., Hossain, N., Saleem, M., Hussain, S., Rasool, L. & Manzoor, H. (2021). Effect of micronutrient and hormone on microalgae growth assessment for biofuel feedstock. Sustainability, 13(9), 5035. https://doi.org/10.3390/ su13095035 google scholar
  • Bashir, K. M. I., Mansoor, S., Kim, N. R., Grohmann, F. R., Shah, A. A., & Cho, M. G. (2019). Effect of organic carbon sources and environmental factors on cell growth and lipid content of Pavlova lutheri. Annals of Microbiology, 69(4), 353-368. https://doi.org/10.1007/s13213-018-1423-2 google scholar
  • Begum, H., Yusoff, F. M., Banerjee, S., Khatoon, H., & Shariff, M. (2016). Availability and utilization of pigments from microalgae. Critical Reviews in Food Science and Nutrition, 56(13), 2209-2222. https:// doi.org/10.1080/10408398.2013.764841 google scholar
  • 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 google scholar
  • Budge, S. M., Parrish, C. C., & Mckenzie, C. H. (2001). Fatty acid composition of phytoplankton, settling particulate matter and sediments at a sheltered bivalve aquaculture site. Marine Chemistry, 76(4), 285-303. https://doi.org/10.1016/S0304-4203(01)00068-8 google scholar
  • Canavate, J. P., & Fernandez-Dıaz, C. (2022). Salinity induces unique changes in lipid classes and fatty acids of the estuarine haptophyte Diacronema vlkianum. European Journal of Phycology, 57(3), 297317. https://doi.org/10.1080/09670262.2021.1970234 google scholar
  • Camacho-Rodrîguez, J., Macıas-Sanchez, M. D., Ceron-Garcıa, M. C., Alarcon, F. J., & Molina-Grima, E. (2018). Microalgae as a potential ingredient for partial fish meal replacement in aquafeeds: nutrient stability under different storage conditions. Journal of Applied Phycology, 30, 1049-1059. https://doi.org/10.1007/s10811-017-1281-5 google scholar
  • Chaisutyakorn, P., Praiboon, J., & Kaewsuralikhit, C. (2018). The effect of temperature on growth and lipid and fatty acid composition on marine microalgae used for biodiesel production. Journal of Applied Phycology, 30, 37-45. https://doi.org/10.1007/s10811-017-1186-3 google scholar
  • Chen, C. Y., Zhao, X. Q., Yen, H. W., Ho, S. H., Cheng, C. L., Lee, D., Bai, F & Chang, J. S. (2013). Microalgae-based carbohydrates for biofuel production. Biochemical Engineering Journal, 78, 1-10. https://doi. org/10.1016/j.bej.2013.03.006 google scholar
  • Chiu, S. Y., Kao, C. Y., Huang, T. T., Lin, C. J., Ong, S. C., Chen, C. D., Chang, J. & Lin, C. S. (2011). Microalgal biomass production and on-site bioremediation of carbon dioxide, nitrogen oxide and sulfur dioxide from flue gas using Chlorella sp. cultures. Bioresource Technology, 102(19), 9135-9142. https://doi.org/10.1016/j.biortech.2011.06.091 google scholar
  • Christie, W. W. (1982). Lipid analysis (2nd revised ed., p. 201). Oxford: Pergamon Press. google scholar
  • Das, P., Mandal, S. C., Bhagabati, S. K., Akhtar, M. S., & Singh, S. K. (2012). Important live food organisms and their role in aquaculture. Frontiers in Aquaculture, 5(4), 69-86. google scholar
  • da Silva Ferreira, V., & Sant’Anna, C. (2017). Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World Journal of Microbiology and Biotechnology, 33(1), 20. https://doi.org/10.1007/s11274-016-2181-6 google scholar
  • de Souza Celente, G., Rizzetti, T. M., Sui, Y., & de Souza Schneider, R. D. C. (2022). Potential use of microalga Dunaliella salina for bioproducts with industrial relevance. Biomass and Bioenergy, 167, 106647. https://doi.org/10.1016/j.biombioe.2022.106647 google scholar
  • Eryalçın, K. M., Roo, J., Saleh, R., Atalah, E., Benftez, T., Betancor, M., Hernandez-Cruz, M. & Izquierdo, M. (2013). Fish oil replacement by different microalgal products in microdiets for early weaning of gilthead sea bream (Sparus aurata, L.). Aquaculture Research, 44(5), 819-828. https://doi.org/10.1111/j.1365-2109.2012.03237.x google scholar
  • Eryalçın, K. M., & Yıldız, M. (2015). Effects of long-term feeding with dried microalgae added microdiets on growth and fatty acid composition of gilthead sea bream (Sparus aurata L., 1758). Turkish Journal of Fisheries and Aquatic Sciences, 15(4), 905-915. https://doi. org/10.4194/1303-2712-v15_4_14 google scholar
  • Eryalçın, K. M., Ganuza, E., Atalah, E., & Hernândez Cruz, M. C. (2015). Nannochloropsis gaditana and Crypthecodinium cohnii, two microalgae as alternative sources of essential fatty acids in early weaning for gilthead seabream. Hi'drobiologica, 25(2), 193-202. google scholar
  • Eryalçın, K. (2018). Effects of different commercial feeds and enrichments on biochemical composition and fatty acid profile of rotifer (Brachionus plicatilis, Muller 1786) and Artemia franciscana. Turkish Journal of Fisheries and Aquatic Sciences, 18. https://doi. org/10.4194/1303-2712-v18_1_09 google scholar
  • Eryalçın, K. M. (2019). Nutritional value and production performance of the rotifer Brachionus plicatilis Müller, 1786 cultured with different feeds at commercial scale. Aquaculture International, 27(3), 875-890. https://doi.org/10.1007/s10499-019-00375-5 google scholar
  • Fields, M. W., Hise, A., Lohman, E. J., Bell, T., Gardner, R. D., Corredor, L., Characklis, G. & Gerlach, R. (2014). Sources and resources: importance of nutrients, resource allocation, and ecology in microalgal cultivation for lipid accumulation. Applied Microbiology and Biotechnology, 98, 4805-4816. https://doi.org/10.1007/s00253-014-5694-7 google scholar
  • Folch, J., Lees, M., & Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226(1), 497-509. google scholar
  • Fradique, M., Batista, A. P., Nunes, M. C., Gouveia, L., Bandarra, N. M., & Raymundo, A. (2013). Isochrysis galbana and Diacronema vlkianum biomass incorporation in pasta products as PUFA’s source. LWT-Food Science and Technology, 50(1), 312-319. https://doi.org/10.1016/j. lwt.2012.05.006 google scholar
  • Guillard, R. R. (1975). Culture of phytoplankton for feeding marine invertebrates. In Culture of marine invertebrate animals: proceedings—1st conference on culture of marine invertebrate animals greenport (pp. 29-60). Boston, MA: Springer US. google scholar
  • 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. https://doi.org/10.1007/s00449-011-0635-7 google scholar
  • Goh, B. H. H., Ong, H. C., Cheah, M. Y., Chen, W. H., Yu, K. L., & Mahlia, T. M. I. (2019). Sustainability of direct biodiesel synthesis from microalgae biomass: A critical review. Renewable and Sustainable Energy Reviews, 107, 59-74. https://doi.org/10.1016/j.rser.2019.02.012 google scholar
  • Gharajeh, N. H., Valizadeh, M., Dorani, E., & Hejazi, M. A. (2020). Biochemical profiling of three indigenous Dunaliella isolates with main focus on fatty acid composition towards potential biotechnological application. Biotechnology Reports, 26, e00479. https://doi.org/10.1016/j.btre.2020.e00479 google scholar
  • Gu, G., Ou, D., Chen, Z., Gao, S., Sun, S., Zhao, Y., Hu, C., & Liang, X. (2022). Metabolomics revealed the photosynthetic performance and metabolomic characteristics of Euglena gracilis under autotrophic and mixotrophic conditions. World Journal of Microbiology and Biotechnology, 38(9), 160. https://doi.org/10.1007/s11274-022-03346-w google scholar
  • Guedes, A. C., Meireles, L. A., Amaro, H. M., & Malcata, F. X. (2010). Changes in lipid class and fatty acid composition of cultures of Pavlova lutheri, in response to light intensity. Journal of the American Oil Chemists’ Society, 87(7), 791-801. https://doi.org/10.1016/j. btre.2020.e00479 google scholar
  • He, Q., Yang, H., Wu, L., & Hu, C. (2015). Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae. Bioresource Technology, 191, 219-228. https://doi.org/10.1016/j.biortech.2015.05.021 google scholar
  • Hemaiswarya, S., Raja, R., Ravi Kumar, R., Ganesan, V., & Anbazhagan, C. (2011). Microalgae: a sustainable feed source for aquaculture. World Journal of Microbiology and Biotechnology, 27, 1737-1746. https:// doi.org/10.1007/s11274-010-0632-z google scholar
  • Izquierdo, M. S., T. Watanabe, T. Takeuchi, T. Arakawa & C. Kitajima. (1990). Optimal EFA levels in Artemia to meet the EFA requirements of red seabream (Pagrus major). In: Takeda, M. & T. Watanabe. (Eds.). The Current Status of Fish Nutrition in Aquaculture. Tokyo University Fisheries, Tokyo, pp. 221-232. google scholar
  • Jeong, U., Choi, J. K., Kang, C. M., Choi, B. D., & Kang, S. J. (2016). Effects of culture methods on the growth rates and fatty acid profiles of Euglena gracilis. Korean Journal of Fisheries and Aquatic Sciences, 49(1), 38-44. google scholar
  • Khatoon, H., Rahman, N. A., Suleiman, S. S., Banerjee, S., & Abol-Munafi, A. B. (2019). Growth and proximate composition of Scenedesmus obliquus and Selenastrum bibraianum cultured in different media and condition. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 89, 251-257. https://doi. org/10.1007/s40011-017-0938-9 google scholar
  • Kottuparambil, S., Thankamony, R. L., & Agusti, S. (2019). Euglena as a potential natural source of value-added metabolites. A review. Algal Research, 37, 154-159. https://doi.org/10.1016/j.algal.2018.11.024 google scholar
  • Kumaran, M., Palanisamy, K. M., Bhuyar, P., Maniam, G. P., Rahim, M. H. A., & Govindan, N. (2023). Agriculture of microalgae Chlorella vulgaris for polyunsaturated fatty acids (PUFAs) production employing palm oil mill effluents (POME) for future food, wastewater, and energy nexus. Energy Nexus, 9, 100169. https://doi.org/10.1016/j. nexus.2022.100169 google scholar
  • Lau, Z. L., Low, S. S., Ezeigwe, E. R., Chew, K. W., Chai, W. S., Bhatnagar, A., Yap, Y. & Show, P. L. (2022). A review on the diverse interactions between microalgae and nanomaterials: growth variation, photosynthesis performance and toxicity. Bioresource Technology, 127048. https://doi.org/10.1016/j.biortech.2022.127048 google scholar
  • Liu, Z. Y., Wang, G. C., & Zhou, B. C. (2008). Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresource google scholar
  • Technology, 99(11), 4717-4722. https://doi.org/10.1016/j.biortech.2007.09.073 google scholar
  • Metsoviti, M. N., Papapolymerou, G., Karapanagiotidis, I. T., & Katsoulas, N. (2019). Effect of light intensity and quality on growth rate and composition of Chlorella vulgaris. Plants, 9(1), 31. https://doi. org/10.3390/plants9010031 google scholar
  • Mohsenpour, S. F., & Willoughby, N. (2016). Effect of CO2 aeration on cultivation of microalgae in luminescent photobioreactors. Biomass and Bioenergy, 85, 168-177. https://doi.org/10.1016/j.biombioe.2015.12.002 google scholar
  • Neori, A. (2011). “Green water” microalgae: the leading sector in world aquaculture. Journal of Applied Phycology, 23, 143-149. https://doi. org/10.1007/s10811-010-9531-9 google scholar
  • Nwoye, E. C., Chukwuma, O. J., Obisike, N. O., Shedrack, O. I., & Nwuche, C. O. (2017). Evaluation of some biological activities of Euglena gracilis biomass produced by a fed-batch culture with some crop fertilizers. African Journal of Biotechnology, 16(8), 337-345. https://doi.org/10.5897/AJB2016.15651 google scholar
  • Parrish, C. C., Wells, J. S., Yang, Z., & Dabinett, P. (1998). Growth and lipid composition of scallop juveniles Placopecten magellanicus fed the flagellate Isochrysis galbana with varying lipid composition and the diatom Chaetoceros muelleri. Marine Biology, 133, 461-471. https:// doi.org/10.1007/s002270050486 google scholar
  • Patil, V., Reitan, K. I., Knutsen, G., Mortensen, L. M., Kâllqvist, T., Olsen, E., Vogt, G. & Gisler0d, H. R. (2005). Microalgae as source of polyunsaturated fatty acids for aquaculture. Plant Biology, 6(6), 5765. google scholar
  • Patil, V., Kallqvist, T., Olsen, E., Vogt, G., & Gisler0d, H. R. (2007). Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquaculture International, 15, 1-9. https://doi.org/10.1007/ s10499-006-9060-3 google scholar
  • Pazos, A. J., Roman, G., Acosta, C. P., Sanchez, J. L., & Abad, M. (1997). Lipid classes and fatty acid composition in the female gonad of Pecten maximus in relation to reproductive cycle and environmental variables. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 117(3), 393-402. https://doi. org/10.1016/S0305-0491(97)00135-1 google scholar
  • Peltomaa, E., Johnson, M. D., & Taipale, S. J. (2017). Marine cryptophytes are great sources of EPA and DHA. Marine Drugs, 16(1), 3. https:// doi.org/10.3390/md16010003 google scholar
  • Prochazkova, G., Branyikova, I., Zachleder, V., & Branyik, T. (2014). Effect of nutrient supply status on biomass composition of eukaryotic green microalgae. Journal of Applied Phycology, 26, 1359-1377. https:// doi.org/10.1007/s10811-013-0154-9 google scholar
  • Raja, R., Anbazhagan, C., Lakshmi, D., & Rengasamy, R. (2004). Nutritional studies on Dunaliella salina (Volvocales, Chlorophyta) under laboratory conditions. Seaweed Resources Utilization, 26(1&2), 127146. google scholar
  • Sandnes, J. M., Kâllqvist, T., Wenner, D., & Gisler0d, H. R. (2005). Combined influence of light and temperature on growth rates of Nannochloropsis oceanica: linking cellular responses to large-scale biomass production. Journal of Applied Phycology, 17, 515-525. https://doi.org/10.1007/s10811-005-9002-x google scholar
  • Schwarzhans, J. P., Cholewa, D., Grimm, P., Beshay, U., Risse, J. M., Friehs, K., & Flaschel, E. (2015). Dependency of the fatty acid composition of Euglena gracilis on growth phase and culture conditions. Journal of Applied Phycology, 27, 1389-1399. https://doi.org/10.1007/s10811-014-0458-4 google scholar
  • Shaaban, M. M., El-Saady, A. M., & El-Sayed, A. B. (2010). Green microalgae water extract and micronutrients foliar application as promoters to nutrient balance and growth of wheat plants. Journal of American Science, 6(9), 631-636. google scholar
  • Shah, S. M. U., Che Radziah, C., Ibrahim, S., Latiff, F., Othman, M. F., & Abdullah, M. A. (2014). Effects of photoperiod, salinity and pH on cell growth and lipid content of Pavlova lutheri. Annals of Microbiology, 64(1), 157-164. https://doi.org/10.1007/s13213-013-0645-6 google scholar
  • Shah, M. R., Lutzu, G. A., Alam, A., Sarker, P., Kabir Chowdhury, M. A., Parsaeimehr, A., Liang, Y. & Daroch, M. (2018). Microalgae in aquafeeds for a sustainable aquaculture industry. Journal of Applied Phycology, 30, 197-213. https://doi.org/10.1007/s10811-017-1234-z google scholar
  • Singh, J., & Saxena, R. C. (2015). An introduction to microalgae: diversity and significance. In Handbook of marine Microalgae (pp. 11-24). Academic Press. https://doi.org/10.1016/B978-0-12-800776-1.00002-9 google scholar
  • Soto-Sânchez, O., Hidalgo, P., Gonzâlez, A., Oliveira, P E., Hernândez Arias, A. J., & Dantagnan, P. (2023). Microalgae as raw materials for aquafeeds: Growth kinetics and improvement strategies of polyunsaturated fatty acids production. Aquaculture Nutrition, 2023. https://doi.org/10.1155/2023/5110281 google scholar
  • Spınola, M. P., Costa, M. M., & Prates, J. A. (2023). Enhancing Digestibility of Chlorella vulgaris Biomass in Monogastric Diets: Strategies and Insights. Animals, 13(6), 1017. https://doi.org/10.3390/ani13061017 google scholar
  • Spolaore, P., Joannis-Cassan, C., Duran, E., & Isambert, A. (2006). Commercial applications of microalgae. Journal of Bioscience and Bioengineering, 101(2), 87-96. https://doi.org/10.1263/jbb.101.87 google scholar
  • Taş, B., & Dalkıran, T. G. (2022). Investigation of the Effect of Zero-Valent Iron Nanoparticle on Chlorella sp. Growth in Autotrophic, Mixotrophic and Heterotrophic Cultures. Review of Hydrobiology, 15, 1-20. google scholar
  • 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. https://doi.org/10.1038/ s41598-020-79950-3 google scholar
  • Turcihan, G., Turgay, E., Yardımcı, R. E., & Eryalçın, K. M. (2021). The effect of feeding with different microalgae on survival, growth, and fatty acid composition of Artemia franciscana metanauplii and on predominant bacterial species of the rearing water. Aquaculture International, 29(5), 2223-2241. https://doi.org/10.1007/s10499-021-00745-y google scholar
  • Turcihan, G., Isinibilir, M., Zeybek, Y. G., & Eryalçın, K. M. (2022). Effect of different feeds on reproduction performance, nutritional components and fatty acid composition of cladocer water flea (Daphnia magna). Aquaculture Research, 53(6), 2420-2430. https://doi.org/10.1111/ are.15759 google scholar
  • Wang, Y., Seppânen-Laakso, T., Rischer, H., & Wiebe, M. G. (2018). Euglena gracilis growth and cell composition under different temperature, light and trophic conditions. PLoS One, 13(4), e0195329. https://doi.org/10.1371/journal.pone.0195329 google scholar
  • Wollmann, F., Dietze, S., Ackermann, J. U., Bley, T., Walther, T., Steingroewer, J., & Krujatz, F. (2019). Microalgae wastewater treatment: Biological and technological approaches. Engineering in Life Sciences, 19(12), 860-871. https://doi.org/10.1002/elsc.201900071 google scholar
  • Yeh, K. L., Chang, J. S., & Chen, W. M. (2010). Effect of light supply and carbon source on cell growth and cellular composition of a newly isolated microalga Chlorella vulgaris ESP-31. Engineering in Life Sciences, 10(3), 201-208. https://doi.org/10.1002/elsc.200900116 google scholar
  • Zhang, K., Wan, M., Bai, W., He, M., Wang, W., Fan, F., Guo, J., Yu, T. & Li, Y. (2023). A novel method for extraction of paramylon from Euglena gracilis for industrial production. Algal Research, 71, 103058. https:// doi.org/10.1016/j.algal.2023.103058 google scholar
  • Zhao, B., Zhang, Y., Xiong, K., Zhang, Z., Hao, X., & Liu, T. (2011). Effect of cultivation mode on microalgal growth and CO2 fixation. Chemical Engineering Research and Design, 89(9), 1758-1762. https://doi. org/10.1016/j.cherd.2011.02.018 google scholar
Year 2024, Volume: 39 Issue: 1, 8 - 16, 09.01.2024
https://doi.org/10.26650/ASE20241303511

Abstract

Project Number

FLO-2022-39273

References

  • AOAC (1995). Official methods of analysis of the association of analytical chemistry (15th ed.). Arlington, VA: AOAC. google scholar
  • Ahmed, F., Zhou, W., & Schenk, P. M. (2015). Pavlova lutheri is a high-level producer of phytosterols. Algal Research, 10, 210-217. https://doi. org/10.1016/j.algal.2015.05.013 google scholar
  • Ahmad, M. T., Shariff, M., Md. Yusoff, F., Goh, Y. M., & Banerjee, S. (2020). Applications of microalga Chlorella vulgaris in aquaculture. Reviews in Aquaculture, 12(1), 328-346. https://doi.org/10.1111/raq.12320 google scholar
  • Arkronrat, W., Deemark, P., & Oniam, V. (2016). Growth performance and proximate composition of mixed cultures of marine microalgae (Nannochloropsis sp.& Tetraselmis sp.)withmonocultures. Songklanakarin Journal of Science and Technology, 38(1), 1-5. google scholar
  • Aslam, A., Rasul, S., Bahadar, A., Hossain, N., Saleem, M., Hussain, S., Rasool, L. & Manzoor, H. (2021). Effect of micronutrient and hormone on microalgae growth assessment for biofuel feedstock. Sustainability, 13(9), 5035. https://doi.org/10.3390/ su13095035 google scholar
  • Bashir, K. M. I., Mansoor, S., Kim, N. R., Grohmann, F. R., Shah, A. A., & Cho, M. G. (2019). Effect of organic carbon sources and environmental factors on cell growth and lipid content of Pavlova lutheri. Annals of Microbiology, 69(4), 353-368. https://doi.org/10.1007/s13213-018-1423-2 google scholar
  • Begum, H., Yusoff, F. M., Banerjee, S., Khatoon, H., & Shariff, M. (2016). Availability and utilization of pigments from microalgae. Critical Reviews in Food Science and Nutrition, 56(13), 2209-2222. https:// doi.org/10.1080/10408398.2013.764841 google scholar
  • 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 google scholar
  • Budge, S. M., Parrish, C. C., & Mckenzie, C. H. (2001). Fatty acid composition of phytoplankton, settling particulate matter and sediments at a sheltered bivalve aquaculture site. Marine Chemistry, 76(4), 285-303. https://doi.org/10.1016/S0304-4203(01)00068-8 google scholar
  • Canavate, J. P., & Fernandez-Dıaz, C. (2022). Salinity induces unique changes in lipid classes and fatty acids of the estuarine haptophyte Diacronema vlkianum. European Journal of Phycology, 57(3), 297317. https://doi.org/10.1080/09670262.2021.1970234 google scholar
  • Camacho-Rodrîguez, J., Macıas-Sanchez, M. D., Ceron-Garcıa, M. C., Alarcon, F. J., & Molina-Grima, E. (2018). Microalgae as a potential ingredient for partial fish meal replacement in aquafeeds: nutrient stability under different storage conditions. Journal of Applied Phycology, 30, 1049-1059. https://doi.org/10.1007/s10811-017-1281-5 google scholar
  • Chaisutyakorn, P., Praiboon, J., & Kaewsuralikhit, C. (2018). The effect of temperature on growth and lipid and fatty acid composition on marine microalgae used for biodiesel production. Journal of Applied Phycology, 30, 37-45. https://doi.org/10.1007/s10811-017-1186-3 google scholar
  • Chen, C. Y., Zhao, X. Q., Yen, H. W., Ho, S. H., Cheng, C. L., Lee, D., Bai, F & Chang, J. S. (2013). Microalgae-based carbohydrates for biofuel production. Biochemical Engineering Journal, 78, 1-10. https://doi. org/10.1016/j.bej.2013.03.006 google scholar
  • Chiu, S. Y., Kao, C. Y., Huang, T. T., Lin, C. J., Ong, S. C., Chen, C. D., Chang, J. & Lin, C. S. (2011). Microalgal biomass production and on-site bioremediation of carbon dioxide, nitrogen oxide and sulfur dioxide from flue gas using Chlorella sp. cultures. Bioresource Technology, 102(19), 9135-9142. https://doi.org/10.1016/j.biortech.2011.06.091 google scholar
  • Christie, W. W. (1982). Lipid analysis (2nd revised ed., p. 201). Oxford: Pergamon Press. google scholar
  • Das, P., Mandal, S. C., Bhagabati, S. K., Akhtar, M. S., & Singh, S. K. (2012). Important live food organisms and their role in aquaculture. Frontiers in Aquaculture, 5(4), 69-86. google scholar
  • da Silva Ferreira, V., & Sant’Anna, C. (2017). Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World Journal of Microbiology and Biotechnology, 33(1), 20. https://doi.org/10.1007/s11274-016-2181-6 google scholar
  • de Souza Celente, G., Rizzetti, T. M., Sui, Y., & de Souza Schneider, R. D. C. (2022). Potential use of microalga Dunaliella salina for bioproducts with industrial relevance. Biomass and Bioenergy, 167, 106647. https://doi.org/10.1016/j.biombioe.2022.106647 google scholar
  • Eryalçın, K. M., Roo, J., Saleh, R., Atalah, E., Benftez, T., Betancor, M., Hernandez-Cruz, M. & Izquierdo, M. (2013). Fish oil replacement by different microalgal products in microdiets for early weaning of gilthead sea bream (Sparus aurata, L.). Aquaculture Research, 44(5), 819-828. https://doi.org/10.1111/j.1365-2109.2012.03237.x google scholar
  • Eryalçın, K. M., & Yıldız, M. (2015). Effects of long-term feeding with dried microalgae added microdiets on growth and fatty acid composition of gilthead sea bream (Sparus aurata L., 1758). Turkish Journal of Fisheries and Aquatic Sciences, 15(4), 905-915. https://doi. org/10.4194/1303-2712-v15_4_14 google scholar
  • Eryalçın, K. M., Ganuza, E., Atalah, E., & Hernândez Cruz, M. C. (2015). Nannochloropsis gaditana and Crypthecodinium cohnii, two microalgae as alternative sources of essential fatty acids in early weaning for gilthead seabream. Hi'drobiologica, 25(2), 193-202. google scholar
  • Eryalçın, K. (2018). Effects of different commercial feeds and enrichments on biochemical composition and fatty acid profile of rotifer (Brachionus plicatilis, Muller 1786) and Artemia franciscana. Turkish Journal of Fisheries and Aquatic Sciences, 18. https://doi. org/10.4194/1303-2712-v18_1_09 google scholar
  • Eryalçın, K. M. (2019). Nutritional value and production performance of the rotifer Brachionus plicatilis Müller, 1786 cultured with different feeds at commercial scale. Aquaculture International, 27(3), 875-890. https://doi.org/10.1007/s10499-019-00375-5 google scholar
  • Fields, M. W., Hise, A., Lohman, E. J., Bell, T., Gardner, R. D., Corredor, L., Characklis, G. & Gerlach, R. (2014). Sources and resources: importance of nutrients, resource allocation, and ecology in microalgal cultivation for lipid accumulation. Applied Microbiology and Biotechnology, 98, 4805-4816. https://doi.org/10.1007/s00253-014-5694-7 google scholar
  • Folch, J., Lees, M., & Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226(1), 497-509. google scholar
  • Fradique, M., Batista, A. P., Nunes, M. C., Gouveia, L., Bandarra, N. M., & Raymundo, A. (2013). Isochrysis galbana and Diacronema vlkianum biomass incorporation in pasta products as PUFA’s source. LWT-Food Science and Technology, 50(1), 312-319. https://doi.org/10.1016/j. lwt.2012.05.006 google scholar
  • Guillard, R. R. (1975). Culture of phytoplankton for feeding marine invertebrates. In Culture of marine invertebrate animals: proceedings—1st conference on culture of marine invertebrate animals greenport (pp. 29-60). Boston, MA: Springer US. google scholar
  • 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. https://doi.org/10.1007/s00449-011-0635-7 google scholar
  • Goh, B. H. H., Ong, H. C., Cheah, M. Y., Chen, W. H., Yu, K. L., & Mahlia, T. M. I. (2019). Sustainability of direct biodiesel synthesis from microalgae biomass: A critical review. Renewable and Sustainable Energy Reviews, 107, 59-74. https://doi.org/10.1016/j.rser.2019.02.012 google scholar
  • Gharajeh, N. H., Valizadeh, M., Dorani, E., & Hejazi, M. A. (2020). Biochemical profiling of three indigenous Dunaliella isolates with main focus on fatty acid composition towards potential biotechnological application. Biotechnology Reports, 26, e00479. https://doi.org/10.1016/j.btre.2020.e00479 google scholar
  • Gu, G., Ou, D., Chen, Z., Gao, S., Sun, S., Zhao, Y., Hu, C., & Liang, X. (2022). Metabolomics revealed the photosynthetic performance and metabolomic characteristics of Euglena gracilis under autotrophic and mixotrophic conditions. World Journal of Microbiology and Biotechnology, 38(9), 160. https://doi.org/10.1007/s11274-022-03346-w google scholar
  • Guedes, A. C., Meireles, L. A., Amaro, H. M., & Malcata, F. X. (2010). Changes in lipid class and fatty acid composition of cultures of Pavlova lutheri, in response to light intensity. Journal of the American Oil Chemists’ Society, 87(7), 791-801. https://doi.org/10.1016/j. btre.2020.e00479 google scholar
  • He, Q., Yang, H., Wu, L., & Hu, C. (2015). Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae. Bioresource Technology, 191, 219-228. https://doi.org/10.1016/j.biortech.2015.05.021 google scholar
  • Hemaiswarya, S., Raja, R., Ravi Kumar, R., Ganesan, V., & Anbazhagan, C. (2011). Microalgae: a sustainable feed source for aquaculture. World Journal of Microbiology and Biotechnology, 27, 1737-1746. https:// doi.org/10.1007/s11274-010-0632-z google scholar
  • Izquierdo, M. S., T. Watanabe, T. Takeuchi, T. Arakawa & C. Kitajima. (1990). Optimal EFA levels in Artemia to meet the EFA requirements of red seabream (Pagrus major). In: Takeda, M. & T. Watanabe. (Eds.). The Current Status of Fish Nutrition in Aquaculture. Tokyo University Fisheries, Tokyo, pp. 221-232. google scholar
  • Jeong, U., Choi, J. K., Kang, C. M., Choi, B. D., & Kang, S. J. (2016). Effects of culture methods on the growth rates and fatty acid profiles of Euglena gracilis. Korean Journal of Fisheries and Aquatic Sciences, 49(1), 38-44. google scholar
  • Khatoon, H., Rahman, N. A., Suleiman, S. S., Banerjee, S., & Abol-Munafi, A. B. (2019). Growth and proximate composition of Scenedesmus obliquus and Selenastrum bibraianum cultured in different media and condition. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 89, 251-257. https://doi. org/10.1007/s40011-017-0938-9 google scholar
  • Kottuparambil, S., Thankamony, R. L., & Agusti, S. (2019). Euglena as a potential natural source of value-added metabolites. A review. Algal Research, 37, 154-159. https://doi.org/10.1016/j.algal.2018.11.024 google scholar
  • Kumaran, M., Palanisamy, K. M., Bhuyar, P., Maniam, G. P., Rahim, M. H. A., & Govindan, N. (2023). Agriculture of microalgae Chlorella vulgaris for polyunsaturated fatty acids (PUFAs) production employing palm oil mill effluents (POME) for future food, wastewater, and energy nexus. Energy Nexus, 9, 100169. https://doi.org/10.1016/j. nexus.2022.100169 google scholar
  • Lau, Z. L., Low, S. S., Ezeigwe, E. R., Chew, K. W., Chai, W. S., Bhatnagar, A., Yap, Y. & Show, P. L. (2022). A review on the diverse interactions between microalgae and nanomaterials: growth variation, photosynthesis performance and toxicity. Bioresource Technology, 127048. https://doi.org/10.1016/j.biortech.2022.127048 google scholar
  • Liu, Z. Y., Wang, G. C., & Zhou, B. C. (2008). Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresource google scholar
  • Technology, 99(11), 4717-4722. https://doi.org/10.1016/j.biortech.2007.09.073 google scholar
  • Metsoviti, M. N., Papapolymerou, G., Karapanagiotidis, I. T., & Katsoulas, N. (2019). Effect of light intensity and quality on growth rate and composition of Chlorella vulgaris. Plants, 9(1), 31. https://doi. org/10.3390/plants9010031 google scholar
  • Mohsenpour, S. F., & Willoughby, N. (2016). Effect of CO2 aeration on cultivation of microalgae in luminescent photobioreactors. Biomass and Bioenergy, 85, 168-177. https://doi.org/10.1016/j.biombioe.2015.12.002 google scholar
  • Neori, A. (2011). “Green water” microalgae: the leading sector in world aquaculture. Journal of Applied Phycology, 23, 143-149. https://doi. org/10.1007/s10811-010-9531-9 google scholar
  • Nwoye, E. C., Chukwuma, O. J., Obisike, N. O., Shedrack, O. I., & Nwuche, C. O. (2017). Evaluation of some biological activities of Euglena gracilis biomass produced by a fed-batch culture with some crop fertilizers. African Journal of Biotechnology, 16(8), 337-345. https://doi.org/10.5897/AJB2016.15651 google scholar
  • Parrish, C. C., Wells, J. S., Yang, Z., & Dabinett, P. (1998). Growth and lipid composition of scallop juveniles Placopecten magellanicus fed the flagellate Isochrysis galbana with varying lipid composition and the diatom Chaetoceros muelleri. Marine Biology, 133, 461-471. https:// doi.org/10.1007/s002270050486 google scholar
  • Patil, V., Reitan, K. I., Knutsen, G., Mortensen, L. M., Kâllqvist, T., Olsen, E., Vogt, G. & Gisler0d, H. R. (2005). Microalgae as source of polyunsaturated fatty acids for aquaculture. Plant Biology, 6(6), 5765. google scholar
  • Patil, V., Kallqvist, T., Olsen, E., Vogt, G., & Gisler0d, H. R. (2007). Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquaculture International, 15, 1-9. https://doi.org/10.1007/ s10499-006-9060-3 google scholar
  • Pazos, A. J., Roman, G., Acosta, C. P., Sanchez, J. L., & Abad, M. (1997). Lipid classes and fatty acid composition in the female gonad of Pecten maximus in relation to reproductive cycle and environmental variables. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 117(3), 393-402. https://doi. org/10.1016/S0305-0491(97)00135-1 google scholar
  • Peltomaa, E., Johnson, M. D., & Taipale, S. J. (2017). Marine cryptophytes are great sources of EPA and DHA. Marine Drugs, 16(1), 3. https:// doi.org/10.3390/md16010003 google scholar
  • Prochazkova, G., Branyikova, I., Zachleder, V., & Branyik, T. (2014). Effect of nutrient supply status on biomass composition of eukaryotic green microalgae. Journal of Applied Phycology, 26, 1359-1377. https:// doi.org/10.1007/s10811-013-0154-9 google scholar
  • Raja, R., Anbazhagan, C., Lakshmi, D., & Rengasamy, R. (2004). Nutritional studies on Dunaliella salina (Volvocales, Chlorophyta) under laboratory conditions. Seaweed Resources Utilization, 26(1&2), 127146. google scholar
  • Sandnes, J. M., Kâllqvist, T., Wenner, D., & Gisler0d, H. R. (2005). Combined influence of light and temperature on growth rates of Nannochloropsis oceanica: linking cellular responses to large-scale biomass production. Journal of Applied Phycology, 17, 515-525. https://doi.org/10.1007/s10811-005-9002-x google scholar
  • Schwarzhans, J. P., Cholewa, D., Grimm, P., Beshay, U., Risse, J. M., Friehs, K., & Flaschel, E. (2015). Dependency of the fatty acid composition of Euglena gracilis on growth phase and culture conditions. Journal of Applied Phycology, 27, 1389-1399. https://doi.org/10.1007/s10811-014-0458-4 google scholar
  • Shaaban, M. M., El-Saady, A. M., & El-Sayed, A. B. (2010). Green microalgae water extract and micronutrients foliar application as promoters to nutrient balance and growth of wheat plants. Journal of American Science, 6(9), 631-636. google scholar
  • Shah, S. M. U., Che Radziah, C., Ibrahim, S., Latiff, F., Othman, M. F., & Abdullah, M. A. (2014). Effects of photoperiod, salinity and pH on cell growth and lipid content of Pavlova lutheri. Annals of Microbiology, 64(1), 157-164. https://doi.org/10.1007/s13213-013-0645-6 google scholar
  • Shah, M. R., Lutzu, G. A., Alam, A., Sarker, P., Kabir Chowdhury, M. A., Parsaeimehr, A., Liang, Y. & Daroch, M. (2018). Microalgae in aquafeeds for a sustainable aquaculture industry. Journal of Applied Phycology, 30, 197-213. https://doi.org/10.1007/s10811-017-1234-z google scholar
  • Singh, J., & Saxena, R. C. (2015). An introduction to microalgae: diversity and significance. In Handbook of marine Microalgae (pp. 11-24). Academic Press. https://doi.org/10.1016/B978-0-12-800776-1.00002-9 google scholar
  • Soto-Sânchez, O., Hidalgo, P., Gonzâlez, A., Oliveira, P E., Hernândez Arias, A. J., & Dantagnan, P. (2023). Microalgae as raw materials for aquafeeds: Growth kinetics and improvement strategies of polyunsaturated fatty acids production. Aquaculture Nutrition, 2023. https://doi.org/10.1155/2023/5110281 google scholar
  • Spınola, M. P., Costa, M. M., & Prates, J. A. (2023). Enhancing Digestibility of Chlorella vulgaris Biomass in Monogastric Diets: Strategies and Insights. Animals, 13(6), 1017. https://doi.org/10.3390/ani13061017 google scholar
  • Spolaore, P., Joannis-Cassan, C., Duran, E., & Isambert, A. (2006). Commercial applications of microalgae. Journal of Bioscience and Bioengineering, 101(2), 87-96. https://doi.org/10.1263/jbb.101.87 google scholar
  • Taş, B., & Dalkıran, T. G. (2022). Investigation of the Effect of Zero-Valent Iron Nanoparticle on Chlorella sp. Growth in Autotrophic, Mixotrophic and Heterotrophic Cultures. Review of Hydrobiology, 15, 1-20. google scholar
  • 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. https://doi.org/10.1038/ s41598-020-79950-3 google scholar
  • Turcihan, G., Turgay, E., Yardımcı, R. E., & Eryalçın, K. M. (2021). The effect of feeding with different microalgae on survival, growth, and fatty acid composition of Artemia franciscana metanauplii and on predominant bacterial species of the rearing water. Aquaculture International, 29(5), 2223-2241. https://doi.org/10.1007/s10499-021-00745-y google scholar
  • Turcihan, G., Isinibilir, M., Zeybek, Y. G., & Eryalçın, K. M. (2022). Effect of different feeds on reproduction performance, nutritional components and fatty acid composition of cladocer water flea (Daphnia magna). Aquaculture Research, 53(6), 2420-2430. https://doi.org/10.1111/ are.15759 google scholar
  • Wang, Y., Seppânen-Laakso, T., Rischer, H., & Wiebe, M. G. (2018). Euglena gracilis growth and cell composition under different temperature, light and trophic conditions. PLoS One, 13(4), e0195329. https://doi.org/10.1371/journal.pone.0195329 google scholar
  • Wollmann, F., Dietze, S., Ackermann, J. U., Bley, T., Walther, T., Steingroewer, J., & Krujatz, F. (2019). Microalgae wastewater treatment: Biological and technological approaches. Engineering in Life Sciences, 19(12), 860-871. https://doi.org/10.1002/elsc.201900071 google scholar
  • Yeh, K. L., Chang, J. S., & Chen, W. M. (2010). Effect of light supply and carbon source on cell growth and cellular composition of a newly isolated microalga Chlorella vulgaris ESP-31. Engineering in Life Sciences, 10(3), 201-208. https://doi.org/10.1002/elsc.200900116 google scholar
  • Zhang, K., Wan, M., Bai, W., He, M., Wang, W., Fan, F., Guo, J., Yu, T. & Li, Y. (2023). A novel method for extraction of paramylon from Euglena gracilis for industrial production. Algal Research, 71, 103058. https:// doi.org/10.1016/j.algal.2023.103058 google scholar
  • Zhao, B., Zhang, Y., Xiong, K., Zhang, Z., Hao, X., & Liu, T. (2011). Effect of cultivation mode on microalgal growth and CO2 fixation. Chemical Engineering Research and Design, 89(9), 1758-1762. https://doi. org/10.1016/j.cherd.2011.02.018 google scholar
There are 71 citations in total.

Details

Primary Language English
Subjects Hydrobiology
Journal Section Research Article
Authors

Merve Sayar 0000-0002-2628-0608

Kamil Mert Eryalçın 0000-0002-8336-957X

Project Number FLO-2022-39273
Publication Date January 9, 2024
Submission Date May 27, 2023
Published in Issue Year 2024 Volume: 39 Issue: 1

Cite

APA Sayar, M., & Eryalçın, K. M. (2024). Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena gracilis, Chlorella vulgaris) and Marine (Pavlova lutheri, Diacronema vlkanium) Microalgae. Aquatic Sciences and Engineering, 39(1), 8-16. https://doi.org/10.26650/ASE20241303511
AMA Sayar M, Eryalçın KM. Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena gracilis, Chlorella vulgaris) and Marine (Pavlova lutheri, Diacronema vlkanium) Microalgae. Aqua Sci Eng. January 2024;39(1):8-16. doi:10.26650/ASE20241303511
Chicago Sayar, Merve, and Kamil Mert Eryalçın. “Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena Gracilis, Chlorella Vulgaris) and Marine (Pavlova Lutheri, Diacronema Vlkanium) Microalgae”. Aquatic Sciences and Engineering 39, no. 1 (January 2024): 8-16. https://doi.org/10.26650/ASE20241303511.
EndNote Sayar M, Eryalçın KM (January 1, 2024) Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena gracilis, Chlorella vulgaris) and Marine (Pavlova lutheri, Diacronema vlkanium) Microalgae. Aquatic Sciences and Engineering 39 1 8–16.
IEEE M. Sayar and K. M. Eryalçın, “Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena gracilis, Chlorella vulgaris) and Marine (Pavlova lutheri, Diacronema vlkanium) Microalgae”, Aqua Sci Eng, vol. 39, no. 1, pp. 8–16, 2024, doi: 10.26650/ASE20241303511.
ISNAD Sayar, Merve - Eryalçın, Kamil Mert. “Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena Gracilis, Chlorella Vulgaris) and Marine (Pavlova Lutheri, Diacronema Vlkanium) Microalgae”. Aquatic Sciences and Engineering 39/1 (January 2024), 8-16. https://doi.org/10.26650/ASE20241303511.
JAMA Sayar M, Eryalçın KM. Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena gracilis, Chlorella vulgaris) and Marine (Pavlova lutheri, Diacronema vlkanium) Microalgae. Aqua Sci Eng. 2024;39:8–16.
MLA Sayar, Merve and Kamil Mert Eryalçın. “Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena Gracilis, Chlorella Vulgaris) and Marine (Pavlova Lutheri, Diacronema Vlkanium) Microalgae”. Aquatic Sciences and Engineering, vol. 39, no. 1, 2024, pp. 8-16, doi:10.26650/ASE20241303511.
Vancouver Sayar M, Eryalçın KM. Investigation of Growth Performance, Proximate and Fatty Acid Composition of Freshwater (Euglena gracilis, Chlorella vulgaris) and Marine (Pavlova lutheri, Diacronema vlkanium) Microalgae. Aqua Sci Eng. 2024;39(1):8-16.

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