Abstract
The chlorophtye Coccomyxa sp. (strain onubensis) growing under either inorganic phosphorus or sulfur starvation showed, unlike other non-extremophile microalgae, the ability to grow still for a period of 2 weeks with retention of high activity of photosystem II, due to P and S reserves in the microalga. Lutein and β-carotene contents slightly increased for a few days in nitrogen-lacking cultures only, with no major impact on productivity due to cease of growth. Maximum fatty acid content of Coccomyxa sp. (strain onubensis) growing in nutrient-lacking culture media accounted for about 13 % of dry biomass and about 50 % of the total lipid fraction, linolenic (C18:3) being the most abundant fatty acid. The lipid content of this microalga is on the average of non-extremophile microalgae, but it has the advantage of producing in highly acidic culture media (pH 2.5, and even lower) which allow its outdoor production-preserving cultures from other microalgae contamination. Nutrient-limited cultures showed a significant increase in the intracellular activity levels of the enzymes glutathione reductase (GR), ascorbate peroxidase (APX) and catalase (CAT), indicating a connection between nutrient deprivation and oxidative stress in Coccomyxa sp. (strain onubensis).
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References
Antal TK, Lindblad P (2005) Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp PCC 6803 during dark incubation with methane or at various extracellular pH. J Appl Microbiol 98:114–120
Ben-Amotz A (1987) Effects of irradiance and nutrient deficiency on the chemical composition of Dunaliella bardawil Ben-Amotz and Avron (Volvocales, Chlorophyta). J Plant Physiol 131:479–487
Ben-Amotz A, Avron M (1983) On the factors which determine massive β-carotene accumulation in the halotolerant alga Dunaliella bardawil. Plant Physiol 72:593–597
Berden-Zrimec M, Drinovec L, Molinari L, Zrimec A, Umani SF, Monti M (2008) Delayed fluorescence as a measure of nutrient limitation in Dunaliella tertiolecta. J Photochem Photobiol B 92:13–18
Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Phys 37:911–917
Borowitzka MA, Moheimani NR (2013) Open pond culture systems. In: Borowitzka MA, Moheimani NR (eds) Algae for Biofuels and Energy. Springer, Dordrecht, pp 133–152
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cakmak T, Angun P, Demiray YE, Ozkan AD, Elibol Z, Tekinay T (2012) Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol Bioeng 109:1947–1957
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306
Courchesne NMD, Parisien A, BeiWang P, Lan CQ (2009) Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J Biotechnol 141:31–41
Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants, a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
Garbayo I, Cuaresma M, Vílchez C, Vega JM (1998) Effect of abiotic stress on the production of lutein and β-carotene by Chlamydomonas acidophila. Process Biochem 43:1158–1161
Garbayo I, Torronteras R, Forján E, Cuaresma M, Casal C, Mogedas B, Ruiz-Domínguez MC, Márquez C, Vaquero I, Fuentes-Cordero JL, Fuentes R, González-del-Valle M, Vílchez C (2012) Identification and physiological aspects of a novel carotenoid-enriched, metal-resistant microalga isolated from an acidic river in Huelva (Spain). J Phycol 48:607–614
Geider RJ, La Roche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate and iron starvation. J Phycol 29:755–766
Geider RJ, MacIntyre H, Graziano LM, McKay RM (1998) Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur J Phycol 33:315–332
Gross W (2000) Ecophysiology of algae living in highly acidic environments. Hydrobiologia 433:31–37
Guschina IA, Harwood JL (2006) Lipids metabolism in eukaryotic algae. Prog Lipid Res 45:160–186
Halliwell B (1996) Cellular stress and protection mechanisms. Biochem Soc Trans 24:1023–1027
Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstock for biofuel production, perspectives and advances. Plant J 54:621–639
James GO, Hocart CH, Hillier W, Chen H, Kordbacheh F, Price GD, Djordjevic MA (2011) Fatty acid profiling of Chlamydomonas reinhardtii under nitrogen deprivation. Bioresource Technol 102:3343–3351
Kiritsakis AK, Dugan LR (1985) Studies in photooxidation of olive oil. J Am Oil Chem Soc 62:892–896
Lamers PP, Janssen M, De Vosc RCH, Bino RJ, Wijffels RH (2012) Carotenoid and fatty acid metabolism in nitrogen-starved Dunaliella salina, a unicellular green microalga. J Biotechnol 162:21–27
Lers A, Levy H, Zamir A (1991) Co-regulation of a gene homologous to early light-induced genes in higher-plants and beta-carotene biosynthesis in the alga Dunaliella bardawil. J Biol Chem 266:13698–13705
Li M, Hu C, Zhu Q, Chen L, Kong Z, Liu Z (2006) Copper and zinc induction of lipid peroxidation effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 62:565–572
Mandal S, Mallick N (2009) Microalga Scenedesmus obliquus as a potential source for biodiesel production. Appl Microbiol Biotech 84:281–291
Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ 14:217–232
Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136
Mendes A, Reis A, Vasconcelos R, Guerra P, Lopes da Silva T (2009) Crypthecodinium cohnii with emphasis on DHA production: a review. J Appl Phycol 21:119–214
Metzger P, Largeau C (2005) Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl Microbiol Biot 66:486–496
Phadwal K, Singh PK (2003) Effect of nutrient depletion on β-carotene and glycerol accumulation in two strains of Dunaliella sp. Bioresource Technol 90:55–58
Remias D, Lütz-Meindl U, Lütz C (2005) Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur J Phycol 40:259–268
Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil, strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112
Scarsella M (2010) Study on the optimal growing conditions of Chlorella vulgaris in bubble column photobioreactors. Chem Eng T 17:85–90
Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC and Govindjee (Eds.), Chlorophyll Fluorescence: A Signature of Photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 279– 319.
Spijkerman E, Wacker A (2011) Interactions between P-limitation and different C conditions on the fatty acid composition of an extremophile microalga. Extremophiles 15:597–609
Tan Y, Lin J (2011) Biomass production and fatty acid profile of a Scenedesmus rubescens like microalga. Bioresource Technol 102:10131–10135
Tonon T, Harvey D, Larson TR, Graham IA (2002) Long chain polyunsaturated fatty acids production and partitioning to triacylglycerols in four microalgae. Phytochemistry 61:15–24
Vaquero I, Ruiz-Domínguez MC, Márquez M, Vílchez C (2012) Cu-mediated biomass productivity enhancement and lutein enrichment of the novel microalga Coccomyxa onubensis. Process Biochem 47:694–700
Vílchez C, Forján E, Cuaresma M, Bédmar F, Garbayo I, Vega JM (2011) Marine carotenoids: biological functions and commercial applications. Mar Drugs 9:319–333
Volgusheva AA, Zagidullin VE, Antal TK, Korvatovsky BN, Krendeleva TE, Paschenko VZ, Rubin AB (2007) Examination of chlorophyll fluorescence decay kinetics in sulfur deprived algae Chlamydomonas reinhardtii. Biochim Biophys Acta 1767:559–564
Wang B, Zarka A, Trebst A, Boussiba S (2003) Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance. J Phycol 39:1116–1124
Widjaja A, Chien CC, Ju YH (2009) Study of increasing lipid production from fresh water microalgae Chlorella vulgaris. J Taiwan Inst Chem Eng 40:13–20
Wijffels RH, Barbosa MJ, Eppink MHM (2010) Microalgae for the production of bulk chemicals and biofuels. Biofuels Bioprod Biores 4:287–295
Acknowledgments
The authors want to acknowledge the support from Junta de Andalucía (Grant no. AGR-4337, Proyecto de Excelencia) and European Union (FEDER funds) and University of Huelva (POCTEP, I2TEP project). This is contribution No. 65 from the CEIMAR Journal Series.
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Ruiz-Domínguez, M.C., Vaquero, I., Obregón, V. et al. Lipid accumulation and antioxidant activity in the eukaryotic acidophilic microalga Coccomyxa sp. (strain onubensis) under nutrient starvation. J Appl Phycol 27, 1099–1108 (2015). https://doi.org/10.1007/s10811-014-0403-6
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DOI: https://doi.org/10.1007/s10811-014-0403-6