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Screening of microalgae and cyanobacteria strains for α-tocopherol content at different growth phases and the influence of nitrate reduction on α-tocopherol production

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Abstract

Tocopherols (vitamin E) are only synthesized by photosynthetic organisms and have wide applications in cosmetics and as dietary supplements in human nutrition and aquaculture. Tocopherols from microalgae and cyanobacteria are rarely investigated, and little is known about their contents. Therefore, 130 strains of cultured microalgae and cyanobacteria were analyzed for α-tocopherol content under various culture conditions. The growth phase had a significant effect on content of α-tocopherol. Maximal amounts were observed at the stationary growth phase. Reduction of nitrate concentration in media caused an increased production of α-tocopherol. The contents were significantly enhanced when the nitrate concentration was reduced to one fourth in culture media used. The content of α-tocopherol was found to reflect phylogenetic relationships at the level of classes, with classes of Rhodophyta and Cyanobacteria accumulating the lowest contents. Within each class, contents varied widely at the species level emphasizing the importance of extensive screening procedures for the identification of strains with high α-tocopherol contents.

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References

  • Aiba S, Ogawa T (1977) Assessment of growth yield of a blue-green alga, Spirulina platensis, in axenic and continuous culture. J Gen Microbiol 102:179–182

    Article  Google Scholar 

  • Arp G, Bissett A, Brinkmann N, Cousin S, De Beer D, Friedl T, Mohr KI, Neu TR, Reimer A, Shiraishi F, Stackebrandt E, Zippel B (2010) Tufa-forming biofilms of german karstwater streams: microorganisms, exopolymers, hydrochemistry and calcification. Geol Soc Lond, Spec Publ 336:83–118

    Article  CAS  Google Scholar 

  • Bandarra NM, Pereira PA, Batista I, Vilela MH (2003) Fatty acids, sterols and α-tocopherol in Isochrysis galbana. J Food Lipids 10:25–34

    Article  CAS  Google Scholar 

  • Borowitzka MA (1999) Commercial production of microalgae: ponds, tanks, tubes and fermenters. J Biotechnol 70:313–321

    Article  CAS  Google Scholar 

  • Borowitzka MA (2013a) High-value products from microalgae—their development and commercialization. J Appl Phycol 25:743–756

    Article  CAS  Google Scholar 

  • Borowitzka MA (2013b) Energy from microalgae: a short history. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 1–15

    Chapter  Google Scholar 

  • Brown MR, Mular M, Miller I, Farmer C, Trenerry C (1999) The vitamin content of microalgae used in aquaculture. J Appl Phycol 11:247–255

    Article  CAS  Google Scholar 

  • Buono S, Langellotti AL, Martello A, Rinna F, Fogliano V (2014) Functional ingredients from microalgae. Food Funct 5:1669–1685

    Article  CAS  PubMed  Google Scholar 

  • Carballo-Cárdenas EC, Tuan PM, Janssen M, Wijffels RH (2003) Vitamin E (α-tocopherol) production by the marine microalgae Dunaliella tertiolecta and Tetraselmis suecica in batch cultivation. Biomol Eng 20:139–147

    Article  PubMed  Google Scholar 

  • Chacón-Lee T, González-Mariño GE (2010) Microalgae for “healthy” foods—possibilities and challenges. Compr Rev Food Sci Food Saf 9:655–675

    Article  Google Scholar 

  • Chen CY, Zhao XQ, Yen HW, Ho SH, Cheng CL, Lee DJ, Bai FW, Chang JS (2013) Microalgae-based carbohydrates for biofuel production. Biochem Eng J 78:1–10

    Article  CAS  Google Scholar 

  • Chiu A, Kimball AB (2003) Topical vitamins, minerals and botanical ingredients as modulators of environmental and chronological skin damage. Br J Dermatol 149:681–691

    Article  CAS  PubMed  Google Scholar 

  • Cifuentes A, Gonzalez M, Vargas S, Hoeneisen M, Gonzalez N (2003) Optimization of biomass, total carotenoids and astaxanthin production in Haematococcus pluvialis Flotow strain Steptoe (Nevada, USA) under laboratory conditions. Biol Res 36:343–357

    Article  CAS  PubMed  Google Scholar 

  • Cuellar-Bermudez SP, Aguilar-Hernandez I, Cardenas-Chavez DL, Ornelas-Soto N, Romero-Ogawa MA, Parra-Saldivar R (2015) Extraction and purification of high-value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microbial Biotechnol 8:190–209

    Article  CAS  Google Scholar 

  • Culture Collection of Algae at the Goettingen University (SAG), Germany. Available online: http://www.epsag.uni-goettingen.de. Accessed on 10 May 2016

  • Culture Collection of Autotrophic Organisms (CCALA), Czech Republic. Available online: http://www.butbn.cas.cz/ccala/index.php. Accessed on 05 May 2016

  • Damiani MC, Popovich CA, Constenla D, Leonardi PI (2010) Lipid analysis in Haematococcus pluvialis to assess its potential use as a biodiesel feedstock. Bioresour Technol 101:3801–3807

    Article  CAS  PubMed  Google Scholar 

  • Darienko T, Gustavs L, Mudimu O, Rad Menendez C, Schumann R, Karsten U, Friedl T, Pröschold T (2010) Chloroidium, a common terrestrial coccoid green alga previously assigned to Chlorella (Trebouxiophyceae, Chlorophyta). Eur J Phycol 1–17

  • de Jesus Raposo MF, de Morais RMSC, de Morais AMMB (2013) Health applications of bioactive compounds from marine microalgae. Life Sci 93:479–486

    Article  PubMed  Google Scholar 

  • Demirbas A, Fatih Demirbas M (2011) Importance of algae oil as a source of biodiesel. Energy Convers Manag 52:163–170

    Article  Google Scholar 

  • Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 19:235–240

    Article  CAS  PubMed  Google Scholar 

  • Donato M, Vilela MH, Bandarra NM (2003) Fatty acids, sterols, α-tocopherol and total carotenoids composition of Diacronema vulkianum. J Food Lipids 10:267–276

    Article  CAS  Google Scholar 

  • Durmaz Y (2007) Vitamin E (α-tocopherol) production by the marine microalgae Nannochloropsis oculata (Eustigmatophyceae) in nitrogen limitation. Aquaculture 272:717–722

    Article  CAS  Google Scholar 

  • Durmaz Y, Monteiro M, Bandarra N, Gökpinar S, Işik O (2007) The effect of low temperature on fatty acid composition and tocopherols of the red microalga, Porphyridium cruentum. J Appl Phycol 19:223–227

    Article  CAS  Google Scholar 

  • Gómez-Coronado DJM, Ibãnez E, Rupérez FJ, Barbas C (2004) Tocopherol measurement in edible products of vegetable origin. J Chromatogr 1054:227–233

    Article  Google Scholar 

  • Guiry MD (2012) How many species of algae are there? J Phycol 48:1057–1063

    Article  PubMed  Google Scholar 

  • Guschina IA, Harwood JL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45:160–186

    Article  CAS  PubMed  Google Scholar 

  • Gustavs L, Eggert A, Michalik D, Karsten U (2010) Physiological and biochemical responses of green microalgae from different habitats to osmotic and matric stress. Protoplasma 243:3–14

    Article  CAS  PubMed  Google Scholar 

  • Hallmann C, Rüdrich J, Enseleit M, Friedl T, Hoppert M (2011) Microbial diversity on a marble monument: a case study. Environ Earth Sci 63:1701–1711

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639

    Article  CAS  PubMed  Google Scholar 

  • Jensen GS, Ginsberg DI, Drapeau C (2001) Blue-green algae as an immuno-enhancer and biomodulator. JANA 3:24–30

    Google Scholar 

  • Kamal-Eldin A, Appelqvist LÅ (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31:671–701

    Article  CAS  PubMed  Google Scholar 

  • Kivose C, Muramatsu R, Kameyama Y, Ueda T, Igarashi O (1997) Biodiscrimination of α-tocopherol stereoisomers in humans after oral administration. Am J Clin Nutr 65:785–789

    Google Scholar 

  • Kobayashi M, Kakizono T, Nagai S (1991) Astaxanthin production by a green alga, Haematococcus pluvialis accompanied with morphological changes in acetate media. J Ferment Bioeng 71:335–339

    Article  CAS  Google Scholar 

  • Li Z, Keasling JD, Niyogi KK (2012) Overlapping photoprotective function of vitamin E and carotenoids in Chlamydomonas. Plant Physiol 158:313–323

    Article  CAS  PubMed  Google Scholar 

  • Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232

    Article  CAS  Google Scholar 

  • Metting FB (1996) Biodiversity and application of microalgae. J Ind Microbiol Biotechnol 17:477–489

    Article  CAS  Google Scholar 

  • Mokrosnop VM, Polishchuk AV, Zolotareva EK (2016) Accumulation of α-tocopherol and β-carotene in Euglena gracilis cells under autotrophic and mixotrophic culture conditions. Appl Biochem Microbiol 52:216–221

    Article  CAS  Google Scholar 

  • Mudimu O, Rybalka N, Bauersachs T, Friedl T, Schulz R (2015) Influence of different CO2 concentrations on microalgae growth, alpha-tocopherol content and fatty acid composition. Geomicrobiol J 32:291–303

    Article  CAS  Google Scholar 

  • Müller J, Friedl T, Hepperle D, Lorenz M (2005) Distinction between multiple isolates of Chlorella vulgaris (Chlorophyta, Trebouxiophyceae) and testing for conspecificity using amplified fragment length polymorphism and IST rDNA sequences. J Phycol 41:1236–1247

    Article  Google Scholar 

  • Ogbonna JC (2009) Microbiological production of tocopherols: current state and prospects. Appl Microbiol Biotechnol 84:217–225

    Article  CAS  PubMed  Google Scholar 

  • Plaza M, Cifuentes A, Ibáñez E (2008) In the search of new functional food ingredients from algae. Trends Food Sci Technol 19:31–39

    Article  CAS  Google Scholar 

  • Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648

    Article  CAS  PubMed  Google Scholar 

  • Qureshi AA, Bradlow BA, Brace L, Manganello J, Peterson DM, Pearce BC, Wright JJK, Gapor A, Elson CE (1995) Response of hypercholesterolemic subjects to administration of tocotrienols. Lipids 30:1171–1177

    Article  CAS  PubMed  Google Scholar 

  • Rosello Sastre R, Posten C (2010) Die vielfältige Anwendung von Mikroalgen als nachwachsende Rohstoffe. Chem-Ing-Tech 82:1925–1939

    Article  CAS  Google Scholar 

  • Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Woodbury P, Growdon J, Cotman CW, Pfeiffer E, Schneider LS, Thal LJ (1997) A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer’s disease. N Engl J Med 336:1216–1222

    Article  CAS  PubMed  Google Scholar 

  • Shintani D, DellaPenna D (1998) Elevating the vitamin E content of plants through metabolic engineering. Science 282:2098–2100

    Article  CAS  PubMed  Google Scholar 

  • Starr RC, Zeikus JA (1993) UTEX—the culture collection of algae at the University of Texas at Austin. J Phycol 29:1–160

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vismara R, Vestri S, Kusmic C, Barsanti L, Gualtieri P (2003) Natural vitamin E enrichment of Artemia salina fed freshwater and marine microalgae. J Appl Phycol 15:75–80

    Article  CAS  Google Scholar 

  • Wang X, Quinn PJ (1999) Vitamin E and its function in membranes. Prog Lipid Res 38:309–336

    Article  CAS  PubMed  Google Scholar 

  • Wijffels RH (2008) Potential of sponges and microalgae for marine biotechnology. Trends Biotechnol 26:26–31

    Article  CAS  PubMed  Google Scholar 

  • Winckelmann D, Bleeke F, Thomas B, Elle C, Klöck G (2015) Open pond cultures of indigenous algae grown on non-arable land in an arid desert using wastewater. Int Aquat Res 7:221–233

    Article  Google Scholar 

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Acknowledgements

We thank Sandra Pusch for cultivation of the investigated strains and Jens Hermann for the tocopherol analysis. NR and TF acknowledge the assistance in maintenance of the studied strains at the SAG culture collection by Ilse Kunkel, Marlis Heinemann, Hella Timmermann, and Dr. Maike Lorenz.

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Authors and Affiliations

  1. Botanical Institute, Department of Plant Cell Physiology and Biotechnology, Christian-Albrechts-University of Kiel, Am Botanischen Garten 5, D-24118, Kiel, Germany

    Opayi Mudimu, Inga Klara Koopmann & Rüdiger Schulz

  2. Botanical Institute, Department of Plant Ecophysiology, Christian-Albrechts-University of Kiel, Am Botanischen Garten 9, D-24118, Kiel, Germany

    Wolfgang Bilger

  3. Albrecht-von-Haller-Institute, Department of Experimental Phycology and Culture Collection of Algae (SAG), Georg August University of Göttingen, Untere Karspüle 2, 37073, Göttingen, Germany

    Nataliya Rybalka & Thomas Friedl

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  1. Opayi Mudimu
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  2. Inga Klara Koopmann
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  3. Nataliya Rybalka
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  4. Thomas Friedl
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  5. Rüdiger Schulz
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  6. Wolfgang Bilger
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Correspondence to Opayi Mudimu.

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This research was supported by Kompetenzzentrum Biomassenutzung Schleswig-Holstein.

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Mudimu, O., Koopmann, I.K., Rybalka, N. et al. Screening of microalgae and cyanobacteria strains for α-tocopherol content at different growth phases and the influence of nitrate reduction on α-tocopherol production. J Appl Phycol 29, 2867–2875 (2017). https://doi.org/10.1007/s10811-017-1188-1

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  • DOI: https://doi.org/10.1007/s10811-017-1188-1

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