Abstract
Microalgae are considered a sustainable source of high-value products with health benefits. Marine algae-derived omega-3 long-chain polyunsaturated fatty acids (LC-PUFA), such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), are considered dietary elements with effects on mental health, cognition enhancement, and cardiovascular protection. This study investigated the temperature effect on omega-3 LC-PUFA production in eight species of microalgae from various taxonomic groups, with a focus on achieving an optimal balance between omega-3 accumulation and efficient growth performance. Samples were batch-cultivated at four different temperatures, with constant light, and fatty acid methyl esters (FAME) were analyzed by gas chromatography. Several nutritional indices were calculated to assess the potential value of biomass produced for human consumption. Two promising candidates were identified suitable for batch cultivation and large-scale production: Nannochloropsis oculata for EPA and Isochrysis galbana for DHA production, with optimum productivities obtained between 14 and 20 °C, and nutritional indices falling within the range required for nutritional benefit.
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References
Attia YA, Al-Harthi MA, Korish MA, Shiboob MM (2015) Fatty acid and cholesterol profiles and hypocholesterolemic, atherogenic, and thrombogenic indices of table eggs in the retail market. Lipids Health Dis 14:136. https://doi.org/10.1186/s12944-015-0133-z
Babuskin S, Krishnan KR, Babu PAS, Sivarajan M, Sukumar M (2014) Functional foods enriched with marine microalga Nannochloropsis oculata as a source of omega-3 fatty acids. Food Technol Biotechnol 52:292–299
Benvenuti G, Bosma R, Cuaresma M, Janssen M, Barbosa MJ, Wijffels RH (2015) Selecting microalgae with high lipid productivity and photosynthetic activity under nitrogen starvation. J Appl Phycol 27:1425–1431. https://doi.org/10.1007/s10811-014-0470-8
Boelen P, van Dijk R, Damsté JSS, Rijpstra WIC, Buma AG (2013) On the potential application of polar and temperate marine microalgae for EPA and DHA production. AMB Express 3:1–9. https://doi.org/10.1186/2191-0855-3-26
Breuer G, Lamers PP, Martens DE, Wijffels R (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol. Bioresour Technol 124:217–226
Chen C-Y, Nagarajan D, Cheah WY (2018) Eicosapentaenoic acid production from Nannochloropsis oceanica CY2 using deep sea water in outdoor plastic-bag type photobioreactors. Bioresour Technol 253:1–7. https://doi.org/10.1016/J.biortech.2017.12.102
Collos Y (1998) Nitrate uptake, nitrite release and uptake, and new production estimates. Mar Ecol Prog Ser 171:293–301. https://doi.org/10.3354/meps171293
d’Ippolito G, Sardo A, Paris D, Vella F, Adelfi M, Botte P, Gallo C, Fontana A (2015) Potential of lipid metabolism in marine diatoms for biofuel production. Biotechnol Biofuels 8:28. https://doi.org/10.1186/s13068-015-0212-4
Dunstan GA, Brown MR, Volkman JK (2005) Cryptophyceae and Rhodophyceae; chemotaxonomy, phylogeny, and application. Phytochemistry 66:2557–2570. https://doi.org/10.1016/j.phytochem.2005.08.015
Garaffo MA, Vassallo-Agius R, Nengas Y, Lembo E, Rando R, Maisano R, Dugo G, Giuffrida D (2011) Fatty acids profile, atherogenic (IA) and thrombogenic (IT) health lipid indices, of raw roe of blue fin tuna (Thunnus thynnus L.) and their salted product “bottarga”. Food Nutr Sci 2:736–743. https://doi.org/10.4236/fns.2011.27101
Guihéneuf F, Fouqueray M, Mimouni V, Ulmann L, Jacquette B, Tremblin G (2010) Effect of UV stress on the fatty acid and lipid class composition in two marine microalgae Pavlova lutheri (Pavlovophyceae) and Odontella aurita (Bacillariophyceae). J Appl Phycol 22:629–638. https://doi.org/10.1007/s10811-010-9503-0
Guihéneuf F, Stengel DB (2013) LC-PUFA-enriched oil production by microalgae: accumulation of lipid and triacylglycerols containing n-3 LC-PUFA is triggered by nitrogen limitation and inorganic carbon availability in the marine haptophyte Pavlova lutheri. Mar Drugs 11:4246–4266. https://doi.org/10.3390/md11114246
Guschina IA, Harwood JL (2009) Algal lipids and effect of the environment on their biochemistry. In: Arts MT, Brett MT, Kainz M (eds) Lipids in aquatic ecosystems. Springer, New York, pp 1–24
Harwood JL (2004) Membrane lipids in Algae. Lipids Photosynth Struct Funct Genet 6:53–64. https://doi.org/10.1007/0-306-48087-5_3
Hoffmann M, Marxen K, Schulz R, Vanselow KH (2010) TFA and EPA productivities of Nannochloropsis salina influenced by temperature and nitrate stimuli in turbidostatic controlled experiments. Mar Drugs 8:2526–2545. https://doi.org/10.3390/md8092526
Huseby S, Degerlund M, Eriksen GK, Ingebrigtsen RA, Eilertsen HC, Hansen E (2013) Chemical diversity as a function of temperature in six northern diatom species. Mar Drugs 11:4232–4245. https://doi.org/10.3390/md11114232
Ingebrigtsen RA, Hansen E, Andersen JH, Eilertsen HC (2016) Light and temperature effects on bioactivity in diatoms. J Appl Phycol 28:939–950. https://doi.org/10.1007/s10811-015-0631-4
Ivanova JG, Kabaivanova LV, Petkov GD (2015) Temperature and irradiance effects on Rhodella reticulata growth and biochemical characteristics. Russ J Plant Physiol 62:647–652. https://doi.org/10.1134/S102144371504010X
Khoeyi ZA, Seyfabadi J, Ramezanpour Z (2012) Effect of light intensity and photoperiod on biomass and fatty acid composition of the microalgae, Chlorella vulgaris. Aquac Int 20:41–49. https://doi.org/10.1007/s10499-011-9440-1
Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857–865. https://doi.org/10.1046/j.1365-3040.2003.01017.x
Kong P, Du Z, Tang B, Meng Q, Li N (2008) Transgenic production of polyunsaturated fatty acids in mammalian cells. Prog Biochem Biophys 35:1305–1311
Krienitz L, Wirth M (2006) The high content of polyunsaturated fatty acids in Nannochloropsis limnetica (Eustigmatophyceae) and its implication for food web interactions, freshwater aquaculture and biotechnology. Limnologica 36:204–210. https://doi.org/10.1016/j.limno.2006.05.002
Laudadio V, Ceci E, Lastella NMB, Tufarelli V (2015) Dietary high-polyphenols extra-virgin olive oil is effective in reducing cholesterol content in eggs. Lipids Health Dis 14:5. https://doi.org/10.1186/s12944-015-0001-x
Li Y, Ghasemi Naghdi F, Garg S, Adarme-Vega T, Thurecht KJ, Ghafor W, Tannock S, Schenk PM (2014) A comparative study: the impact of different lipid extraction methods on current microalgal lipid research. Microb Cell Factories 13:14. https://doi.org/10.1186/1475-2859-13-14
Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24:300–309
Liu J, Sommerfeld M, Hu Q (2013) Screening and characterization of Isochrysis strains and optimization of culture conditions for docosahexaenoic acid production. Appl Microbiol Biotechnol 97:4785–4798. https://doi.org/10.1007/s00253-013-4749-5
Liu J, Song Y, Qiu W (2017) Oleaginous microalgae Nannochloropsis as a new model for biofuel production: review & analysis. Renew Sust Energ Rev 72:154–162. https://doi.org/10.1016/j.rser.2016.12.120
Molina Grima E, Sánchez Pérez JA, García Sánchez JL, García Camacho F, López Alonso D (1992) EPA from Isochrysis galbana. Growth conditions and productivity. Process Biochem 27:299–305. https://doi.org/10.1016/0032-9592(92)85015-T
Moortele S (1998) Physiopathologie de l’athérosclérose - Mécanismes et prévention de l’athérothrombose. Option Bio 208:6–7
Mulders KJM, Lamers PP, Martens DE, Wijffels RH (2014) Phototrophic pigment production with microalgae: biological constraints and opportunities. J Phycol 50:229–242. https://doi.org/10.1111/jpy.12173
Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Aschwin E, Varela J (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935. https://doi.org/10.3390/md10091920
Poisson L, Ergan F (2001) Docosahexaenoic acid ethyl esters from Isochrysis galbana. J Biotechnol 91:75–81. https://doi.org/10.1016/S0168-1656(01)00295-4
Popova T, Ignatova M, Petkov E, Stanišic N (2016) Difference in fatty acid composition and related nutritional indices of meat between two lines of slow-growing chickens slaughtered at different ages. Arch Anim Breed 59:319–327. https://doi.org/10.5194/aab-59-319-2016
Ragan MA, Bird CJ, Rice EL, Gutell RR, Murphy CA, Singh RK (1994) A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene. Proc Natl Acad Sci U S A 91:7276–7280. https://doi.org/10.1073/pnas.91.15.7276
Renaud SM, Thinh L-V, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195–214. https://doi.org/10.1016/S0044-8486(01)00875-4
Robertson R, Guihéneuf F, Schmid M, Stengel DB, Fitzgerald G, Ross P, Stanton C (2013) Algae-derived polyunsaturated fatty acids: implications for human health. In: Catalá A (ed) Polyunsaturated fatty acids sources, antioxidant properties and health Benefits. Nova Sciences Publishers, Inc., Hauppauge, NY, 11788 USA, pp 45–99
Sanz-Luque E, Chamizo-Ampudia A, Llamas A, Galvan A, Fernandez E (2015) Understanding nitrate assimilation and its regulation in microalgae. Front Plant Sci 6:899. https://doi.org/10.3389/fpls.2015.00899
Sauer J (2001) Nitrogen starvation-induced chlorosis in Synechococcus PCC 7942. Low-level photosynthesis as a mechanism of long-term survival. Plant Physiol 126:233–243. https://doi.org/10.1104/pp.126.1.233
Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553. https://doi.org/10.3390/en5051532
Šimat V, Bogdanović T, Poljak V, Petričević S (2015) Changes in fatty acid composition, atherogenic and thrombogenic health lipid indices and lipid stability of Bogue (Boops boops Linnaeus, 1758) during storage on ice: effect of fish farming activities. J Food Compos Anal 40:120–125. https://doi.org/10.1016/j.jfca.2014.12.026
Solovchenko A (2010) Photoprotection in plants - Optical screening-based mechanisms. Springer-Verlag, Berlin, Heidelberg
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96. https://doi.org/10.1263/jbb.101.87
Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol Adv 29:483–501. https://doi.org/10.1016/j.biotechadv.2011.05.016
Sukenik A (1991) Ecophysiological considerations in the optimization of eicosapentaenoic acid production by Nannochloropsis sp. (Eustigmatophyceae). Bioresour Technol 35:263–269. https://doi.org/10.1016/0960-8524(91)90123-2
Sukenik A, Zmora O, Carmeli Y (1993) Biochemical quality of marine unicellular algae with special emphasis on lipid composition. II. Nannochloropsis sp. Aquaculture 117:313–326. https://doi.org/10.1016/0044-8486(93)90328-V
Thompson PA, Guo M, Harrison PJ, Whyte JNC (1992) Effects of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. J Phycol 28:488–497. https://doi.org/10.1111/j.0022-3646.1992.00488.x
Tonon T, Harvey D, Larson TR, Graham IA (2002) Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae. Phytochemistry 61:15–24. https://doi.org/10.1016/S0031-9422(02)00201-7
Veloza AJ, Chu FLE, Tang KW (2006) Trophic modification of essential fatty acids by heterotrophic protists and its effects on the fatty acid composition of the copepod Acartia tonsa. Mar Biol 148:779–788. https://doi.org/10.1007/s00227-005-0123-1
Faraloni C, Torzillo G (2017) Synthesis of antioxidant carotenoids in microalgae in response to physiological stress. In: Nikolic G (ed) Carotenoids. IntechOpen, pp 143–157. https://doi.org/10.5772/67843
Acknowledgements
This work was supported by SMART FOOD Science based Intelligent/Functional and Medical Foods for Optimum Brain Health, Targeting Depression and Cognition.
Funding
This study was funded by the Department of Agriculture, Food and the Marine of Ireland (grant number ref. no. 13F 411).
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Aussant, J., Guihéneuf, F. & Stengel, D.B. Impact of temperature on fatty acid composition and nutritional value in eight species of microalgae. Appl Microbiol Biotechnol 102, 5279–5297 (2018). https://doi.org/10.1007/s00253-018-9001-x
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DOI: https://doi.org/10.1007/s00253-018-9001-x