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Potential of Microalgae Carotenoids for Industrial Application

  • Eleane A. Cezare-Gomes
  • Lauris del Carmen Mejia-da-Silva
  • Lina S. Pérez-Mora
  • Marcelo C. Matsudo
  • Lívia S. Ferreira-Camargo
  • Anil Kumar Singh
  • João Carlos Monteiro de CarvalhoEmail author
Article
  • 118 Downloads

Abstract

Microalgae cultivation, when compared to the growth of higher plants, presents many advantages such as faster growth, higher biomass productivity, and smaller land area requirement for cultivation. For this reason, microalgae are an alternative platform for carotenoid production when compared to the traditional sources. Currently, commercial microalgae production is not well developed but, fortunately, there are several studies aiming to make the large-scale production feasible by, for example, employing different cultivation systems. This review focuses on the main carotenoids from microalgae, comparing them to the traditional sources, as well as a critical analysis about different microalgae cultivation regimes that are currently available and applicable for carotenoid accumulation. Throughout this review paper, we present relevant information about the main commercial microalgae carotenoid producers; the comparison between carotenoid content from food, vegetables, fruits, and microalgae; and the great importance and impact of these molecule applications, such as in food (nutraceuticals and functional foods), cosmetics and pharmaceutical industries, feed (colorants and additives), and healthcare area. Lastly, the different operating systems applied to these photosynthetic cultivations are critically discussed, and conclusions and perspectives are made concerning the best operating system for acquiring high cell densities and, consequently, high carotenoid accumulation.

Keywords

Carotenoids Carotenoid sources Microalgae Microalgae application Cultivation process 

Notes

Acknowledgments

The authors acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2017/24486-0) for the fellowship.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Xu, L., Weathers, P. J., Xiong, X. R., & Liu, C. Z. (2009). Microalgal bioreactors: challenges and opportunities. Engineering in Life Sciences, 9(3), 178–189.  https://doi.org/10.1002/elsc.200800111.CrossRefGoogle Scholar
  2. 2.
    Walker, T. L., Purton, S., Becker, D. K., & Collet, C. (2005). Microalgae as bioreactors. Plant Cell Reports, 24(11), 629–641.  https://doi.org/10.1007/s00299-005-0004-6.CrossRefPubMedGoogle Scholar
  3. 3.
    Gouveia, L., & Oliveira, A. C. (2009). Microalgae as a raw material for biofuels production. Journal of Industrial Microbiology and Biotechnology, 36(2), 269–274.  https://doi.org/10.1007/s10295-008-0495-6.CrossRefPubMedGoogle Scholar
  4. 4.
    Gupta, P. L., Lee, S. M., & Choi, H. J. (2015). A mini review: Photobioreactors for large scale algal cultivation. World Journal of Microbiology and Biotechnology, 31(9), 1409–1417.  https://doi.org/10.1007/s11274-015-1892-4.CrossRefPubMedGoogle Scholar
  5. 5.
    Chiu, H. F., Liao, J. Y., Lu, Y. Y., Han, Y. C., Shen, Y. C., Venkatakrishnan, K., Golovinskaia, O., & Wang, C. K. (2017). Anti-proliferative, anti-inflammatory and pro-apoptotic effects of Dunaliella salina on human KB oral carcinoma cells. Journal of Food Biochemistry, 41(3), 1–8.  https://doi.org/10.1111/jfbc.12349.CrossRefGoogle Scholar
  6. 6.
    Fimbres-Olivarria, D., Carvajal-Millan, E., Lopez-Elias, J. A., Martinez-Robinson, K. G., Miranda-Baeza, A., Martinez-Cordova, L. R., Enriquez-Ocaña, F., & Valdez-Holguin, J. E. (2017). Chemical characterization and antioxidant activity of sulfated polysaccharides from Navicula sp. Food Hydrocolloids, 75, 229–236.  https://doi.org/10.1016/j.foodhyd.2017.08.002.CrossRefGoogle Scholar
  7. 7.
    Rosenberg, J. N., Oyler, G. A., Wilkinson, L., & Betenbaugh, M. J. (2008). A green light for engineered algae: redirecting metabolism to fuel a biotechnology revolution. Current Opinion in Biotechnology, 19(5), 430–436.  https://doi.org/10.1016/j.copbio.2008.07.008.CrossRefPubMedGoogle Scholar
  8. 8.
    Gantar, M., & Svirčev, Z. (2008). Microalgae and cyanobacteria: food for thought. Journal of Phycology, 44(2), 260–268.  https://doi.org/10.1111/j.1529-8817.2008.00469.x.CrossRefPubMedGoogle Scholar
  9. 9.
    Berman, J., Zorrilla-López, U., Farré, G., Zhu, C., Sandmann, G., Twyman, R. M., Capell, T., & Christou, P. (2015). Nutritionally important carotenoids as consumer products. Phytochemistry Reviews, 14(5), 727–743.  https://doi.org/10.1007/s11101-014-9373-1.CrossRefGoogle Scholar
  10. 10.
    Singh, R. N., & Sharma, S. (2012). Development of suitable photobioreactor for algae production—a review. Renewable and Sustainable Energy Reviews, 16(4), 2347–2353.  https://doi.org/10.1016/j.rser.2012.01.026.CrossRefGoogle Scholar
  11. 11.
    Del Campo, J. A., García-González, M., & Guerrero, M. G. (2007). Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Applied Microbiology and Biotechnology, 74(6), 1163–1174.  https://doi.org/10.1007/s00253-007-0844-9.CrossRefPubMedGoogle Scholar
  12. 12.
    Moreno-garcia, L., Adjallé, K., Barnabé, S., & Raghavan, G. S. V. (2017). Microalgae biomass production for a biorefinery system: recent advances and the way towards sustainability. Renewable and Sustainable Energy Reviews, 76, 493–506.  https://doi.org/10.1016/j.rser.2017.03.024.CrossRefGoogle Scholar
  13. 13.
    Fernandes, B. D., Mota, A., Teixeira, J. A., & Vicente, A. A. (2015). Continuous cultivation of photosynthetic microorganisms: approaches, applications and future trends. Biotechnology Advances, 33(6), 1228–1245.CrossRefPubMedGoogle Scholar
  14. 14.
    Morales-Sánchez, D., Martinez-Rodriguez, O. A., & Martinez, A. (2017). Heterotrophic cultivation of microalgae: production of metabolites of commercial interest. Journal of Chemical Technology and Biotechnology, 92(5), 925–936.  https://doi.org/10.1002/jctb.5115.CrossRefGoogle Scholar
  15. 15.
    Carvalho, J. C. M., Bezerra, R. P., Matsudo, M. C., & Sato, S. (2013). Cultivation of Arthrospira (Spirulina) platensis by fed-batch process. In J. W. Lee (Ed.), Advanced biofuels and bioproducts (pp. 781–805). New York: Springer.  https://doi.org/10.1007/978-1-4614-3348-4.CrossRefGoogle Scholar
  16. 16.
    Saini, R. K., Nile, S. H., & Park, S. W. (2015). Carotenoids from fruit and vegetables: chemistry, analysis, occurrence, bioavailability and biological activities. Food Research International, 76, 735–750.  https://doi.org/10.1016/j.aqpro.2013.07.003.CrossRefPubMedGoogle Scholar
  17. 17.
    Shi, X. M., Jiang, Y., & Chen, F. (2002). High-yield production of lutein by the green microalga Chlorella protothecoides in heterotrophic fed-batch culture. Biotechnology Progress, 18(4), 723–727.  https://doi.org/10.1021/bp0101987.CrossRefPubMedGoogle Scholar
  18. 18.
    Lorenz, R. T., & Cysewski, G. R. (2000). Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends in Biotechnology, 18(4), 160–167.CrossRefPubMedGoogle Scholar
  19. 19.
    Gong, M., & Bassi, A. (2016). Carotenoids from microalgae: a review of recent developments. Biotechnology Advances, 34(8), 1396–1412.  https://doi.org/10.1016/j.biotechadv.2016.10.005.CrossRefPubMedGoogle Scholar
  20. 20.
    Business Communications Company (2015). The global market for carotenoids—code – FOD025E. Retrieved October 23, 2017, from https://www.bccresearch.com/market-research/food-and-beverage/carotenoids-global-market-report-fod025e.html
  21. 21.
    Rasala, B. A., & Mayfield, S. P. (2015). Photosynthetic biomanufacturing in green algae; production of recombinant proteins for industrial, nutritional, and medical uses. Photosynthesis Research, 123(3), 227–239.  https://doi.org/10.1007/s11120-014-9994-7.CrossRefPubMedGoogle Scholar
  22. 22.
    Peng, J., Yuan, J. P., Wu, C. F., & Wang, J. H. (2011). Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: metabolism and bioactivities relevant to human health. Marine Drugs, 9(10), 1806–1828.  https://doi.org/10.3390/md9101806.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Gammone, M. A., & D’Orazio, N. (2015). Anti-obesity activity of the marine carotenoid fucoxanthin. Marine Drugs, 13(4), 2196–2214.  https://doi.org/10.3390/md13042196.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Yaakob, Z., Ali, E., Zainal, A., Mohamad, M., & Takriff, M. S. (2014). An overview: Biomolecules from microalgae for animal feed and aquaculture. Journal of Biological Research (Greece), 21(1), 1–10.  https://doi.org/10.1186/2241-5793-21-6.CrossRefGoogle Scholar
  25. 25.
    Grobbelaar, J. U. (2016). AUFWIND: an ambitious German microalgae project for producing third-generation biofuels. South African Journal of Science, 112(9–10), 9–10.  https://doi.org/10.17159/sajs.2016/a0174.CrossRefGoogle Scholar
  26. 26.
    Prasanna, R., & Kaushik, B. D. (2010). Evolutionary relationships among cyanobacteria, algae and plants: revisited in the light of Darwinism. In V. P. Sharma (Ed.), Nature at work: ongoing saga of evolution (pp. 119–140). New Delhi: Springer.CrossRefGoogle Scholar
  27. 27.
    Gimpel, J. A., Henríquez, V., & Mayfield, S. P. (2015). In metabolic engineering of eukaryotic microalgae: potential and challenges come with great diversity. Frontiers in Microbiology, 6(DEC), 1–14.  https://doi.org/10.3389/fmicb.2015.01376.CrossRefGoogle Scholar
  28. 28.
    Hemaiswarya, S., Raja, R., Ravikumar, R., & Carvalho, I. S. (2013). Microalgae taxonomy and breeding. Biofuel crops: production, physiology and genetics, (January 2016), 44–53. Retrieved from https://www.researchgate.net/publication/286617872
  29. 29.
    Norton, T. A., Melkonian, M., & Andersen, R. A. (1996). Algal biodiversity*. Phycologia, 35(4), 308–326.  https://doi.org/10.2216/i0031-8884-35-4-308.1.CrossRefGoogle Scholar
  30. 30.
    McCann, A. E., & Cullimore, D.. (1979). Residue reviews. In F. A. Gunther (Ed.), Influence of pesticides on soil algal flora (pp. 1–31). Riverside: Springer.Google Scholar
  31. 31.
    Chisti, Y. (2007). Biodiesel from microalgae. Biotechnology Advances, 25(3), 294–306.  https://doi.org/10.1016/j.biotechadv.2007.02.001.CrossRefPubMedGoogle Scholar
  32. 32.
    Boyce, D. G., Lewis, M. R., & Worm, B. (2010). Global phytoplankton decline over the past century. Nature, 466(7306), 591–596.  https://doi.org/10.1038/nature09268.CrossRefPubMedGoogle Scholar
  33. 33.
    Algaebase. (n.d.). AlgaBase. Retrieved November 17, 2018, from http://www.algaebase.org/
  34. 34.
    García-Balboa, C., Baselga-Cervera, B., García-Sanchez, A., Igual, J. M., Lopez-Rodas, V., & Costas, E. (2013). Rapid adaptation of microalgae to bodies of water with extreme pollution from uranium mining: an explanation of how mesophilic organisms can rapidly colonise extremely toxic environments. Aquatic Toxicology, 144–145, 116–123.  https://doi.org/10.1016/j.aquatox.2013.10.003.CrossRefPubMedGoogle Scholar
  35. 35.
    Brock, T. D., Science, S., Series, N., & Feb, N. (2014). Lower pH limit for the existence of blue-green algae: evolutionary and ecological implications., 179(4072), 480–483.Google Scholar
  36. 36.
    Sakshaug, E., & Slagstad, D. (1991). Light and productivity of phytoplankton in polar marine ecosystems: a physiological view. Polar Research, 10(1), 69–86.  https://doi.org/10.1111/j.1751-8369.1991.tb00636.x.CrossRefGoogle Scholar
  37. 37.
    Pushkareva, E., Johansen, J. R., & Elster, J. (2016). A review of the ecology, ecophysiology and biodiversity of microalgae in Arctic soil crusts. Polar Biology, 39(12), 2227–2240.  https://doi.org/10.1007/s00300-016-1902-5.CrossRefGoogle Scholar
  38. 38.
    Negro, J. J., & Garrido-Fernández, J. (2000). Astaxanthin is the major carotenoid in tissues of white storks (Ciconia ciconia) feeding on introduced crayfish (Procambarus clarkii). Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology, 126(3), 347–352.  https://doi.org/10.1016/S0305-0491(00)00180-2.CrossRefPubMedGoogle Scholar
  39. 39.
    Chandi, G. K., & Gill, B. S. (2011). Production and characterization of microbial carotenoids as an alternative to synthetic colors: a review. International Journal of Food Properties, 14(3), 503–513.  https://doi.org/10.1080/10942910903256956.CrossRefGoogle Scholar
  40. 40.
    Bhosale, P., & Bernstein, P. S. (2005). Microbial xanthophylls. Applied Microbiology and Biotechnology, 68(4), 445–455.  https://doi.org/10.1007/s00253-005-0032-8.CrossRefPubMedGoogle Scholar
  41. 41.
    Eonseon, J., Lee, C.-G., & Polle, J. E. W. (2006). Secondary carotenoid accumulation in Haematococcus Chlorophyceae: biosynthesis, regulation, and biotechnology. Journal of Microbiology and Biotechnology, 16(6), 821–831 Retrieved from http://cat.inist.fr/?aModele=afficheN&cpsidt=17872039.Google Scholar
  42. 42.
    Ye, Z. W., Jiang, J. G., & Wu, G. H. (2008). Biosynthesis and regulation of carotenoids in Dunaliella: progresses and prospects. Biotechnology Advances, 26(4), 352–360.  https://doi.org/10.1016/j.biotechadv.2008.03.004.CrossRefPubMedGoogle Scholar
  43. 43.
    Schmidt-Dannert, C. (2000). Engineering novel carotenoids in microorganisms. Current Opinion in Biotechnology, 11(3), 255–261.  https://doi.org/10.1016/S0958-1669(00)00093-8.CrossRefPubMedGoogle Scholar
  44. 44.
    Grünewald, K., Eckert, M., Hirschberg, J., & Hagen, C. (2000). Phytoene desaturase is localized exclusively in the chloroplast and up-regulated at the mRNA level during accumulation of secondary carotenoids in Haematococcus pluvialis (Volvocales, Chlorophyceae). Plant Physiology, 122(4), 1261–1268.  https://doi.org/10.1104/pp.122.4.1261.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Collins, A. M., Jones, H. D. T., Han, D., Hu, Q., Beechem, T. E., & Timlin, J. A. (2011). Carotenoid distribution in living cells of Haematococcus pluvialis (Chlorophyceae). PLoS One, 6(9), 1–7.  https://doi.org/10.1371/journal.pone.0024302.CrossRefGoogle Scholar
  46. 46.
    Lemoine, Y., & Schoefs, B. (2010). Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynthesis Research, 106(1–2), 155–177.  https://doi.org/10.1007/s11120-010-9583-3.CrossRefPubMedGoogle Scholar
  47. 47.
    Ghosh, A., Khanra, S., Mondal, M., Halder, G., Tiwari, O. N., Saini, S., Bhowmick, T. K., & Gayen, K. (2016). Progress toward isolation of strains and genetically engineered strains of microalgae for production of biofuel and other value added chemicals: a review. Energy Conversion and Management, 113, 104–118.  https://doi.org/10.1016/j.enconman.2016.01.050.CrossRefGoogle Scholar
  48. 48.
    Rosello Sastre, R., & Posten, C. (2010). The variety of microalgae applications as renewable source. Chemie Ingenieur Technik, 82(11), 1925–1939.  https://doi.org/10.1002/cite.201000124.CrossRefGoogle Scholar
  49. 49.
    Borowitzka, M. A. (1992). Algal biotechnology products and processes—matching science and economics. Journal of Applied Phycology, 4(3), 267–279.  https://doi.org/10.1007/BF02161212.CrossRefGoogle Scholar
  50. 50.
    Borowitzka, M. A. (2013). High-value products from microalgae—their development and commercialisation. Journal of Applied Phycology, 25(3), 743–756.  https://doi.org/10.1007/s10811-013-9983-9.CrossRefGoogle Scholar
  51. 51.
    Deinove (n.d.). Carotenoids market. Natural carotenoids meeting consumer needs. Retrieved November 17, 2018, from http://www.deinove.com/en/profile/strategy-and-markets/carotenoids-market
  52. 52.
    Li, J., Zhu, D., Niu, J., Shen, S., & Wang, G. (2011). An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnology Advances, 29(6), 568–574.  https://doi.org/10.1016/j.biotechadv.2011.04.001.CrossRefPubMedGoogle Scholar
  53. 53.
    Nguyen, K. D. (2013). Astaxanthin: a comparative case of synthetic vs. natural production. Chemical and Biomolecular Engineering Publications and Other Works, 1–9. Retrieved from http://trace.tennessee.edu/cgi/viewcontent.cgi?article=1094&context=utk_chembiopubs
  54. 54.
    Lin, J. H., Lee, D. J., & Chang, J. S. (2015). Lutein production from biomass: marigold flowers versus microalgae. Bioresource Technology, 184, 421–428.  https://doi.org/10.1016/j.biortech.2014.09.099.CrossRefPubMedGoogle Scholar
  55. 55.
    Grama, B. S., Chader, S., Khelifi, D., Agathos, S. N., & Jeffryes, C. (2014). Induction of canthaxanthin production in a Dactylococcus microalga isolated from the algerian sahara. Bioresource Technology, 151, 297–305.  https://doi.org/10.1016/j.biortech.2013.10.073.CrossRefPubMedGoogle Scholar
  56. 56.
    Boudreault, G., Cortin, P., Corriveau, L. A., Rousseau, A. P., Tardif, Y., & Malenfant, M. (1983). Canthaxanthine retinopathy: 1. Clinical study in 51 consumers. Canadian Journal of Ophthalmology, 18(7), 325–328.PubMedGoogle Scholar
  57. 57.
    Hsu, Y. W., Tsai, C. F., Chang, W. H., Ho, Y. C., Chen, W. K., & Lu, F. J. (2008). Protective effects of Dunaliella salina—a carotenoids-rich alga, against carbon tetrachloride-induced hepatotoxicity in mice. Food and Chemical Toxicology, 46(10), 3311–3317.  https://doi.org/10.1016/j.fct.2008.07.027.CrossRefPubMedGoogle Scholar
  58. 58.
    Hu, C. C., Lin, J. T., Lu, F. J., Chou, F. P., & Yang, D. J. (2008). Determination of carotenoids in Dunaliella salina cultivated in Taiwan and antioxidant capacity of the algal carotenoid extract. Food Chemistry, 109(2), 439–446.  https://doi.org/10.1016/j.foodchem.2007.12.043.CrossRefPubMedGoogle Scholar
  59. 59.
    Borowitzka, L. J., Borowitzka, M. A., & Moulton, T. P. (1984). The mass culture of Dunaliella for fine chemicals: from laboratory to pilot plant. Hydrobiologia, 116/117(1), 115–134.  https://doi.org/10.1007/BF00027649.CrossRefGoogle Scholar
  60. 60.
    Lamers, P. P., Janssen, M., De Vos, R. C. H., Bino, R. J., & Wijffels, R. H. (2008). Exploring and exploiting carotenoid accumulation in Dunaliella salina for cell-factory applications. Trends in Biotechnology, 26(11), 631–638.  https://doi.org/10.1016/j.tibtech.2008.07.002.CrossRefPubMedGoogle Scholar
  61. 61.
    Aasen, I. M., Ertesvåg, H., Heggeset, T. M. B., Liu, B., Brautaset, T., Vadstein, O., & Ellingsen, T. E. (2016). Thraustochytrids as production organisms for docosahexaenoic acid (DHA), squalene, and carotenoids. Applied Microbiology and Biotechnology, 100(10), 4309–4321.  https://doi.org/10.1007/s00253-016-7498-4.CrossRefPubMedGoogle Scholar
  62. 62.
    Guerin, M., Huntley, M. E., & Olaizola, M. (2003). Haematococcus astaxanthin: applications for human health and nutrition. Trends in Biotechnology, 21(5), 210–216.  https://doi.org/10.1016/S0167-7799(03)00078-7.CrossRefPubMedGoogle Scholar
  63. 63.
    Kang, C. D., Lee, J. S., Park, T. H., & Sim, S. J. (2005). Comparison of heterotrophic and photoautotrophic induction on astaxanthin production by Haematococcus pluvialis. Applied Microbiology and Biotechnology, 68(2), 237–241.  https://doi.org/10.1007/s00253-005-1889-2.CrossRefPubMedGoogle Scholar
  64. 64.
    Zhang, W., Wang, J., Wang, J., & Liu, T. (2014). Attached cultivation of Haematococcus pluvialis for astaxanthin production. Bioresource Technology, 158, 329–335.  https://doi.org/10.1016/j.biortech.2014.02.044.CrossRefPubMedGoogle Scholar
  65. 65.
    Sarada, R., Vidhyavathi, R., Usha, D., & Ravishankar, G. A. (2006). An efficient method for extraction of astaxanthin from green alga Haematococcus pluvialis. Journal of Agricultural and Food Chemistry, 54(20), 7585–7588.  https://doi.org/10.1021/jf060737t.CrossRefPubMedGoogle Scholar
  66. 66.
    Cardozo, K. H. M., Guaratini, T., Barros, M. P., Falcão, V. R., Tonon, A. P., Lopes, N. P., Campos, S., Torres, M. A., Souza, A. O., Colepicolo, P., & Pinto, E. (2007). Metabolites from algae with economical impact. Comparative Biochemistry and Physiology - C Toxicology and Pharmacology, 146(1–2), 60–78.  https://doi.org/10.1016/j.cbpc.2006.05.007.CrossRefPubMedGoogle Scholar
  67. 67.
    Zhang, X., Pan, L., Wei, X., Gao, H., & Liu, J. (2007). Impact of astaxanthin-enriched algal powder of Haematococcus pluvialis on memory improvement in BALB/c mice. Environmental Geochemistry and Health, 29(6), 483–489.  https://doi.org/10.1007/s10653-007-9117-x.CrossRefPubMedGoogle Scholar
  68. 68.
    Shi, X.-M., & Chen, F. (2002). High-yield production of lutein by the green microalga Chlorella protothecoides in heterotrophic fed-batch culture. Biotechnology Progress, 18(4), 723–727.  https://doi.org/10.1021/bp0101987.CrossRefPubMedGoogle Scholar
  69. 69.
    Basu, H. N., Del Vecchio, A. J., Flider, F., & Orthoefer, F. T. (2001). Nutritional and potential disease prevention properties of carotenoids. JAOCS, Journal of the American Oil Chemists’ Society, 78(7), 665–675.  https://doi.org/10.1007/s11746-001-0324-x.CrossRefGoogle Scholar
  70. 70.
    Del Campo, J. A., Rodríguez, H., Moreno, J., Vargas, M. Á., Rivas, J., & Guerrero, M. G. (2001). Lutein production by Muriellopsis sp. in an outdoor tubular photobioreactor. Journal of Biotechnology, 85(3), 289–295.  https://doi.org/10.1016/S0168-1656(00)00380-1.CrossRefPubMedGoogle Scholar
  71. 71.
    Sun, Z., Li, T., Zhou, Z., & Jiang, Y. (2015). Microalgae as a source of lutein: chemistry, biosynthesis, and carotenogenesis. Adv Biochem Eng Biotechnol, 153, 37–58.  https://doi.org/10.1007/10_2015_331.CrossRefGoogle Scholar
  72. 72.
    Chagas, A. L., Rios, A. O., Jarenkow, A., Marcílio, N. R., Ayub, M. A. Z., & Rech, R. (2015). Production of carotenoids and lipids by Dunaliella tertiolecta using CO2 from beer fermentation. Process Biochemistry, 50(6), 981–988.  https://doi.org/10.1016/j.procbio.2015.03.012.CrossRefGoogle Scholar
  73. 73.
    Abe, K., Hattori, H., & Hirano, M. (2007). Accumulation and antioxidant activity of secondary carotenoids in the aerial microalga Coelastrella striolata var. multistriata. Food Chemistry, 100(2), 656–661.  https://doi.org/10.1016/j.foodchem.2005.10.026.CrossRefGoogle Scholar
  74. 74.
    Beatty, S., Boulton, M., Henson, D., Koh, H. H., & Murray, I. J. (1999). Macular pigment and age related macular degeneration. The British Journal of Ophthalmology, 83(7), 867–877.  https://doi.org/10.1136/bjo.83.7.867.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Koo, S. Y., Cha, K. H., Song, D. G., Chung, D., & Pan, C. H. (2012). Optimization of pressurized liquid extraction of zeaxanthin from Chlorella ellipsoidea. Journal of Applied Phycology, 24(4), 725–730.  https://doi.org/10.1007/s10811-011-9691-2.CrossRefGoogle Scholar
  76. 76.
    Ferruzzi, M. G., & Blakeslee, J. (2007). Digestion, absorption, and cancer preventative activity of dietary chlorophyll derivatives. Nutrition Research, 27(1), 1–12.  https://doi.org/10.1016/j.nutres.2006.12.003.CrossRefGoogle Scholar
  77. 77.
    Kim, M., Ahn, J., Jeon, H., Jin, E. S., Cutignano, A., & Romano, G. (2017). Development of a Dunaliella tertiolecta strain with increased zeaxanthin content using random mutagenesis. Marine Drugs, 15(6).  https://doi.org/10.3390/md15060189.
  78. 78.
    Jin, E. S., Feth, B., & Melis, A. (2003). A mutant of the green alga Dunaliella salina constitutively accumulates zeaxanthin under all growth conditions. Biotechnology and Bioengineering, 81(1), 115–124.  https://doi.org/10.1002/bit.10459.CrossRefPubMedGoogle Scholar
  79. 79.
    Bone, R. A., Landrum, J. T., Guerra, L. H., & Ruiz, C. A. (2003). Lutein and zeaxanthin dietary supplements raise macular pigment density and serum concentrations of these carotenoids in humans. The Journal of Nutrition, 133(4), 992–998 Retrieved from http://jn.nutrition.org/content/133/4/992.full.pdf.CrossRefPubMedGoogle Scholar
  80. 80.
    Schubert, N., García-Mendoza, E., & Pacheco-Ruiz, I. (2006). Carotenoid composition of marine red algae. Journal of Phycology, 42(6), 1208–1216.  https://doi.org/10.1111/j.1529-8817.2006.00274.x.CrossRefGoogle Scholar
  81. 81.
    Mishra, N., & Mishra, N. (2018). Exploring the biologically active metabolites of Isochrysis galbana in pharmaceutical interest: an overview. International Journal of Pharmaceutical Sciences and Research, 9(6), 2162–2174.  https://doi.org/10.13040/IJPSR.0975-8232.9(6).2162-74.CrossRefGoogle Scholar
  82. 82.
    Kim, S. M., Kang, S. W., Kwon, O. N., Chung, D., & Pan, C. H. (2012). Fucoxanthin as a major carotenoid in Isochrysis aff. galbana: characterization of extraction for commercial application. Journal of the Korean Society for Applied Biological Chemistry, 55(4), 477–483.  https://doi.org/10.1007/s13765-012-2108-3.CrossRefGoogle Scholar
  83. 83.
    Lu, X., Sun, H., Zhao, W., Cheng, K., Chen, F., & Liu, B. (2018). A hetero-photoautotrophic two-stage cultivation process for production of fucoxanthin by the marine diatom Nitzschia laevis. Marine Drugs, 16(7), 219.  https://doi.org/10.3390/md16070219.CrossRefPubMedCentralGoogle Scholar
  84. 84.
    Ishika, T., Moheimani, N. R., Bahri, P. A., Laird, D. W., Blair, S., & Parlevliet, D. (2017). Halo-adapted microalgae for fucoxanthin production: effect of incremental increase in salinity. Algal Research, 28, 66–73.  https://doi.org/10.1016/j.algal.2017.10.002.CrossRefGoogle Scholar
  85. 85.
    Molina-Miras, A., López-rosales, L., Sánchez-mirón, A., & Cerón-garcía, M. C. (2018). Long-term culture of the marine dinoflagellate microalga Amphidinium carterae in an indoor LED-lighted raceway photobioreactor: production of carotenoids and fatty acids. Bioresource Technology, 265, 257–267.CrossRefPubMedGoogle Scholar
  86. 86.
    Assunção, J., Catarina Guedes, A., & Xavier Malcata, F. (2017). Biotechnological and pharmacological applications of biotoxins and other bioactive molecules from dinoflagellates. Marine Drugs, 15(12).  https://doi.org/10.3390/md15120393.
  87. 87.
    Sugawara, T., Yamashita, K., Sakai, S., Asai, A., Nagao, A., Shiraishi, T., Imai, I., & Hirata, T. (2007). Induction of apoptosis in DLD-1 human colon cancer cells by peridinin isolated from the dinoflagellate, Heterocapsa triquetra. Bioscience, Biotechnology, and Biochemistry, 71(4), 1069–1072.  https://doi.org/10.1271/bbb.60597.CrossRefPubMedGoogle Scholar
  88. 88.
    Benstein, R. M., Çebi, Z., Podola, B., & Melkonian, M. (2014). Immobilized growth of the peridinin-producing marine dinoflagellate Symbiodinium in a simple biofilm photobioreactor. Marine Biotechnology, 16(6), 621–628.  https://doi.org/10.1007/s10126-014-9581-0.CrossRefPubMedGoogle Scholar
  89. 89.
    Ishikawa, C., Jomori, T., Tanaka, J., Senba, M., & Mori, N. (2016). Peridinin, a carotenoid, inhibits proliferation and survival of HTLV-1-infected T-cell lines. International Journal of Oncology, 49(4), 1713–1721.  https://doi.org/10.3892/ijo.2016.3648.CrossRefPubMedGoogle Scholar
  90. 90.
    Cyanotech (n.d.). BioAstin® Hawaiian Astaxanthin®. Retrieved November 17, 2018, from https://www.cyanotech.com/astaxanthin/
  91. 91.
    Algatechnologies (n.d.). Our microalgae. Retrieved November 17, 2018, from https://www.algatech.com/
  92. 92.
    Nature Beta Technologies. (n.d.). Retrieved November 17, 2018, from http://wondercare.co.in/nature/nature.html
  93. 93.
    AquaCarotene (2014). Plankton Australia Pty Limited. Retrieved November 17, 2018, from http://www.planktonaustralia.com/
  94. 94.
    Esatbeyoglu, T., & Rimbach, G. (2017). Canthaxanthin: from molecule to function. Molecular Nutrition and Food Research, 61(6), 1–17.  https://doi.org/10.1002/mnfr.201600469.CrossRefGoogle Scholar
  95. 95.
    Sommerburg, O., Keunen, J. E., Bird, A. C., & van Kuijk, F. J. (1998). Fruits and vegetables that are sources for lutein and zeaxanthin: the macular pigment in human eyes. The British Journal of Ophthalmology, 82(8), 907–910.  https://doi.org/10.1136/BJO.82.8.907.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Piccaglia, R., Marotti, M., & Grandi, S. (1998). Lutein and lutein ester content in different types of Tagetes patula and T. erecta. Industrial Crops and Products, 8(1), 45–51.  https://doi.org/10.1016/S0926-6690(97)10005-X.CrossRefGoogle Scholar
  97. 97.
    Holden, J. M., Eldridge, A. L., Beecher, G. R., Marilyn Buzzard, I., Bhagwat, S., Davis, C. S., Douglass, L. W., Gebhardt, S., Haytowitz, D., & Schakel, S. (1999). Carotenoid content of U.S. foods: an update of the database. Journal of Food Composition and Analysis, 12(3), 169–196.  https://doi.org/10.1006/jfca.1999.0827.CrossRefGoogle Scholar
  98. 98.
    Kopsell, D. A., Lefsrud, M. G., Kopsell, D. E., Wenzel, A. J., Gerweck, C., & Curran-Celentano, J. (2006). Spinach cultigen variation for tissue carotenoid concentrations influences human serum carotenoid levels and macular pigment optical density following a 12-week dietary intervention. Journal of Agricultural and Food Chemistry, 54(21), 7998–8005.  https://doi.org/10.1021/jf0614802.CrossRefPubMedGoogle Scholar
  99. 99.
    Lu, Q. Y., Arteaga, J. R., Zhang, Q., Huerta, S., Go, V. L. W., & Heber, D. (2005). Inhibition of prostate cancer cell growth by an avocado extract: role of lipid-soluble bioactive substances. Journal of Nutritional Biochemistry, 16(1), 23–30.  https://doi.org/10.1016/j.jnutbio.2004.08.003.CrossRefPubMedGoogle Scholar
  100. 100.
    Nishiyama, I., Fukuda, T., & Oota, T. (2007). Cultivar difference in chlorophyll, lutein and β-carotene content in the fruit of kiwifruit and other actinidia species. Acta Horticulturae, 753, 473–478.CrossRefGoogle Scholar
  101. 101.
    Moros, E. E., Darnoko, D., Cheryan, M., Perkins, E. G., & Jerrell, J. (2002). Analysis of xanthophylls in corn by HPLC. Journal of Agricultural and Food Chemistry, 50(21), 5787–5790.  https://doi.org/10.1021/jf020109l.CrossRefPubMedGoogle Scholar
  102. 102.
    Perry, A., Rasmussen, H., & Johnson, E. J. (2009). Xanthophyll (lutein, zeaxanthin) content in fruits, vegetables and corn and egg products. Journal of Food Composition and Analysis, 22(1), 9–15.  https://doi.org/10.1016/j.jfca.2008.07.006.CrossRefGoogle Scholar
  103. 103.
    Sajilata, M. G., Singhal, R. S., & Kamat, M. Y. (2008). The carotenoid pigment zeaxanthin—a review. Comprehensive Reviews in Food Science and Food Safety, 7(1), 29–49.  https://doi.org/10.1111/j.1541-4337.2007.00028.x.CrossRefGoogle Scholar
  104. 104.
    Seddon, J., Ajani, U., & Sperduto, R. (1994). Dietary carotenoids, vitamins A, C, and E, and advanced age-related macular degeneration. J. Am. J. Med. Assoc., 272(18), 1413–1420. Retrieved from http://archpsyc.jamanetwork.com/article.aspx?articleid=382145.CrossRefGoogle Scholar
  105. 105.
    Lin, T. M., Durance, T. D., & Scaman, C. H. (1998). Characterization of vacuum microwave, air and freeze dried carrot slices. Food Research International, 31(2), 111–117.  https://doi.org/10.1016/S0963-9969(98)00070-2.CrossRefGoogle Scholar
  106. 106.
    Favacho, F. S., Lima, J. S. S., Neto, F. B., Silva, J. N., & Barros, A. P. (2017). Productive and economic efficiency of carrot intercropped with cowpea vegetable resulting from green manure and different spatial arrangements. Revista Ciencia Agronomica, 48(2), 337–346.  https://doi.org/10.5935/1806-6690.20170039.CrossRefGoogle Scholar
  107. 107.
    Frusciante, L., Carli, P., Ercolano, M. R., Pernice, R., Di Matteo, A., Fogliano, V., & Pellegrini, N. (2007). Antioxidant nutritional quality of tomato. Molecular Nutrition and Food Research, 51(5), 609–617.  https://doi.org/10.1002/mnfr.200600158.CrossRefPubMedGoogle Scholar
  108. 108.
    Shi, J., & Le Maguer, M. (2000). Lycopene in tomatoes: chemical and physical properties affected by food processing. Critical Reviews in Food Science and Nutrition, 40(1), 1–42.  https://doi.org/10.1080/10408690091189275.CrossRefPubMedGoogle Scholar
  109. 109.
    Renju, G. L., Muraleedhara Kurup, G., & Bandugula, V. R. (2014). Effect of lycopene isolated from Chlorella marina on proliferation and apoptosis in human prostate cancer cell line PC-3. Tumour Biology: the journal of the International Society for Oncodevelopmental Biology and Medicine, 35(11), 10747–10758.  https://doi.org/10.1007/s13277-014-2339-5.CrossRefGoogle Scholar
  110. 110.
    Renju, G. L., Kurup, G. M., & Kumari, C. H. S. (2013). Anti-inflammatory activity of lycopene isolated from Chlorella marina on type II collagen induced arthritis in Sprague Dawley rats. Immunopharmacology and Immunotoxicology, 35(2), 282–291.  https://doi.org/10.3109/08923973.2012.742534.CrossRefPubMedGoogle Scholar
  111. 111.
    Saini, R. K., & Keum, Y.-S. (2018). Carotenoid extraction methods: a review of recent developments. Food Chemistry, 240, 90–103.  https://doi.org/10.1016/j.foodchem.2017.07.099.CrossRefPubMedGoogle Scholar
  112. 112.
    Edge, R., McGarvey, D. J., & Truscott, T. G. (1997). The carotenoids as anti-oxidants—a review. Journal of Photochemistry and Photobiology. B, Biology, 41(3), 189–200.  https://doi.org/10.1016/S1011-1344(97)00092-4.CrossRefPubMedGoogle Scholar
  113. 113.
    Chuang, W. C., Ho, Y. C., Liao, J. W., & Lu, F. J. (2014). Dunaliella salina exhibits an antileukemic immunity in a mouse model of WEHI-3 leukemia cells. Journal of Agricultural and Food Chemistry, 62(47), 11479–11487.  https://doi.org/10.1021/jf503564b.CrossRefPubMedGoogle Scholar
  114. 114.
    Jayappriyan, K. R., Rajkumar, R., Venkatakrishnan, V., Nagaraj, S., & Rengasamy, R. (2013). In vitro anticancer activity of natural β-carotene from Dunaliella salina EU5891199 in PC-3 cells. Biomedicine & Preventive Nutrition, 3(2), 99–105.  https://doi.org/10.1016/j.bionut.2012.08.003.CrossRefGoogle Scholar
  115. 115.
    Sheu, M.-J., Huang, G.-J., Wu, C.-H., Chen, J.-S., Chang, H.-Y., Chang, S.-J., & Chung, J.-G. (2008). Ethanol extract of Dunaliella salina induces cell cycle arrest and apoptosis in A549 human non-small cell lung cancer cells. In Vivo, 22(3), 369–378.PubMedGoogle Scholar
  116. 116.
    Grung, M., D’Souza, F. M. L., Borowitzka, M., & Liaaen-Jensen, S. (1992). Algal carotenoids 51. Secondary carotenoids 2. Haematococcus pluvialis aplanospores as a source of (3S, 3′S)-astaxanthin esters. Journal of Applied Phycology, 4(2), 165–171.  https://doi.org/10.1007/BF02442465.CrossRefGoogle Scholar
  117. 117.
    Rao, A. R., Sindhuja, H. N., Dharmesh, S. M., Sankar, K. U., Sarada, R., & Ravishankar, G. A. (2013). Effective inhibition of skin cancer, tyrosinase, and antioxidative properties by astaxanthin and astaxanthin esters from the green alga Haematococcus pluvialis. Journal of Agricultural and Food Chemistry, 61(16), 3842–3851.  https://doi.org/10.1021/jf304609j.CrossRefPubMedGoogle Scholar
  118. 118.
    Otton, R., Marin, D. P., Bolin, A. P., dos Santos, R. d. C. M., Polotow, T. G., Sampaio, S. C., & de Barros, M. P. (2010). Astaxanthin ameliorates the redox imbalance in lymphocytes of experimental diabetic rats. Chemico-Biological Interactions, 186(3), 306–315.  https://doi.org/10.1016/j.cbi.2010.05.011.CrossRefPubMedGoogle Scholar
  119. 119.
    Monroy-Ruiz, J., Sevilla, M.-Á., Carrón, R., & Montero, M.-J. (2011). Astaxanthin-enriched-diet reduces blood pressure and improves cardiovascular parameters in spontaneously hypertensive rats. Pharmacological Research: the official journal of the Italian Pharmacological Society, 63(1), 44–50.  https://doi.org/10.1016/j.phrs.2010.09.003.CrossRefGoogle Scholar
  120. 120.
    Kläui, H. (1982). Industrial and commercial uses of carotenoids. Carotenoid chemistry and biochemistry. International Union of Pure and Applied Chemistry.  https://doi.org/10.1016/B978-0-08-026224-6.50026-7.
  121. 121.
    Dwyer, J. H., Navab, M., Dwyer, K. M., Hassan, K., Sun, P., Shircore, A., Hama-Levy, S., Hough, G., Wang, X., Drake, T., Merz, C. N. B., & Fogelman, A. M. (2001). Oxygenated carotenoid lutein and progression of early atherosclerosis: the Los Angeles Atherosclerosis Study. Circulation, 103(24), 2922–2927.  https://doi.org/10.1161/01.CIR.103.24.2922.CrossRefPubMedGoogle Scholar
  122. 122.
    Le Marchand, L., Hankin, J. H., Kolonel, L. N., Beecher, G. R., Wilkens, L. R., & Zhao, L. P. (1993). Intake of specific carotenoids and lung cancer risk. Cancer Epidemiology, Biomarkers & Prevention, 2, 183–187.Google Scholar
  123. 123.
    Ziegler, R. G., Elizabeth, A., Hartge, P., Mcadams, J., Janet, B., Mason, T. J., & Fraumeni, J. F. (1996). The importance of alpha-carotene, beta-carotene, and other phytochemicals in the etiology of lung cancer. Journal of the National Cancer Institute, 88(9).Google Scholar
  124. 124.
    Chiu, C. J., & Taylor, A. (2007). Nutritional antioxidants and age-related cataract and maculopathy. Experimental Eye Research, 84(2), 229–245.  https://doi.org/10.1016/j.exer.2006.05.015.CrossRefPubMedGoogle Scholar
  125. 125.
    Schnebelen-Berthier, C., Acar, N., Pouillart, P., Thabuis, C., Rodriguez, B., Depeint, F., Clerc, E., Mathiaud, A., Bourdillon, A., Baert, B., Bretillon, L., & Lecerf, J.-M. (2015). Incorporation of lutein and docosahexaenoic acid from dietary microalgae into the retina in quail. International Journal of Food Sciences and Nutrition, 66(2), 222–229.  https://doi.org/10.3109/09637486.2014.971227.CrossRefPubMedGoogle Scholar
  126. 126.
    Olmedilla, B., Granado, F., Blanco, I., Vaquero, M., & Cajigal, C. (2001). Lutein in patients with cataracts and age-related macular degeneration: a long-term supplementation study. Journal of the Science of Food and Agriculture, 81(9), 904–909.  https://doi.org/10.1002/jsfa.905.CrossRefGoogle Scholar
  127. 127.
    Wei, D., Chen, F., Chen, G., Zhang, X., Liu, L., & Zhang, H. (2008). Enhanced production of lutein in heterotrophic Chlorella protothecoides by oxidative stress. Science in China, Series C: Life Sciences, 51(12), 1088–1093.  https://doi.org/10.1007/s11427-008-0145-2.CrossRefGoogle Scholar
  128. 128.
    Suhonen, R., & Plosila, M. (1981). The effect of beta-carotene in combination with canthaxanthin, Ro 8-8427 (Phenoro), in treatment of polymorphous light eruptions., 163, 172–176.Google Scholar
  129. 129.
    Gensler, H. L., & Holladay, K. (1990). Enhanced resistance to an antigenic tumor in immunosuppressed mice by dietary retinyl palmitate canthaxanthin. Cancer Letter, 49, 231–236.CrossRefGoogle Scholar
  130. 130.
    Ernst, H. (2002). Recent advances in industrial carotenoid synthesis*. Pure and Applied Chemistry, 74(11), 2213–2226.CrossRefGoogle Scholar
  131. 131.
    Malis, S. A., Cohen, E., & Ben Amotz, A. (1993). Accumulation of canthaxanthin in Chlorella emersonii. Physiologia Plantarum, 87(2), 232–236.  https://doi.org/10.1111/j.1399-3054.1993.tb00148.x.CrossRefGoogle Scholar
  132. 132.
    Hanagata, N., & Dubinsky, Z. (1999). Secondary carotenoid accumulation in Scenedesmus komarekii (Chlorophycea, Chlorophyta). Journal of Phycology, 35(5), 960–966.  https://doi.org/10.1046/j.1529-8817.1999.3550960.x.CrossRefGoogle Scholar
  133. 133.
    Pelah, D., Sintov, A., & Cohen, E. (2004). The effect of salt stress on the production of canthaxanthin and astaxanthin by Chlorella zofingiensis grown under limited light intensity. World Journal of Microbiology and Biotechnology, 20(5), 483–486.  https://doi.org/10.1023/B:WIBI.0000040398.93103.21.CrossRefGoogle Scholar
  134. 134.
    Bar, E., Rise, M., Vishkautsan, M., & Arad, S. M. (1995). Pigment and structural changes in Chlorella zofingiensis upon light and nitrogen stress. Journal of Plant Physiology, 146(4), 527–534.  https://doi.org/10.1016/S0176-1617(11)82019-5.CrossRefGoogle Scholar
  135. 135.
    Liu, J., Sun, Z., Gerken, H., Liu, Z., Jiang, Y., & Chen, F. (2014). Chlorella zofingiensis as an alternative microalgal producer of astaxanthin: biology and industrial potential. Marine Drugs, 12(6), 3487–3515.  https://doi.org/10.3390/md12063487.CrossRefPubMedPubMedCentralGoogle Scholar
  136. 136.
    Chen, J. h., Liu, L., & Wei, D. (2017). Enhanced production of astaxanthin by Chromochloris zofingiensis in a microplate-based culture system under high light irradiation. Bioresource Technology, 245, 518–529.  https://doi.org/10.1016/j.biortech.2017.08.102.CrossRefPubMedGoogle Scholar
  137. 137.
    Jansen, R. J., Robinson, D. P., Stolzenberg-solomon, R. Z., William, R., De Andrade, M., Oberg, A. L., Rabe, K. G., Anderson, K. E., Olson, J. E., Sinha, R., & Petersen, G. M. (2014). Nutrients from fruit and vegetable consumption reduce the risk of pancreatic cancer. Journal of Gastrointestinal Cancer, 44(2), 152–161.  https://doi.org/10.1007/s12029-012-9441-y.Nutrients.CrossRefGoogle Scholar
  138. 138.
    Chew, E. Y., Clemons, T. E., SanGiovanni, J. P., Danis, R., Ferris, F. L., III, Elman, M., et al. (2013). Lutein + zeaxanthin and omega-3 fatty acids for age-related macular degeneration. Journal of the American Medical Association, 309(19), 2005–2015.  https://doi.org/10.1001/jama.2013.4997.CrossRefGoogle Scholar
  139. 139.
    Trumbo, P. R., & Ellwood, K. C. (2018). Lutein and zeaxanthin intakes and risk of age-related macular degeneration and cataracts: an evaluation using the Food and Drug Administration’s evidence-based review system for health claims 1–3. The American Journal of Clinical Nutrition, 84, 971–974.CrossRefGoogle Scholar
  140. 140.
    Bone, R. A., Landrum, J. T., Hime, G. W., & Cains, A. (1993). Stereochemistry of the human macular carotenoids. Investigative Ophthalmology & Visual Science, 34(6), 2033–2040.Google Scholar
  141. 141.
    Bernstein, P. S., Li, B., Vachali, P. P., Gorusupudi, A., Shyam, R., Henriksen, B. S., & Nolan, J. M. (2015). Progress in retinal and eye research lutein, zeaxanthin, and meso-zeaxanthin: the basic and clinical science underlying carotenoid-based nutritional interventions against ocular disease. Progress in Retinal and Eye Research, 50, 34–66.  https://doi.org/10.1016/j.preteyeres.2015.10.003.CrossRefPubMedPubMedCentralGoogle Scholar
  142. 142.
    Maccarrone, M., Bari, M., Gasperi, V., & Demmig-Adams, B. (2005). The photoreceptor protector zeaxanthin induces cell death in neuroblastoma cells. Anticancer Research, 25(6B), 3871–3876.PubMedGoogle Scholar
  143. 143.
    Kwang, H. C., Song, Y. I. K., & Lee, D. U. (2008). Antiproliferative effects of carotenoids extracted from Chlorella ellipsoidea and Chlorella vulgaris on human colon cancer cells. Journal of Agricultural and Food Chemistry, 56(22), 10521–10526.  https://doi.org/10.1021/jf802111x.CrossRefGoogle Scholar
  144. 144.
    Othman, R., Mohd Zaifuddin, F. A., & Hassan, N. M. (2014). Carotenoid biosynthesis regulatory mechanisms in plants. Journal of Oleo Science, 63(8), 753–760.  https://doi.org/10.5650/jos.ess13183.CrossRefPubMedGoogle Scholar
  145. 145.
    Rebolloso Fuentes, M. M., Acién Fernández, G. G., Sánchez Pérez, J. A., & Guil Guerrero, J. L. (2000). Biomass nutrient profiles of the microalga Porphyridium cruentum. Food Chemistry, 70(3), 345–353.  https://doi.org/10.1016/S0308-8146(00)00101-1.CrossRefGoogle Scholar
  146. 146.
    Juin, C., Oliveira Junior, R. G. de, Fleury, A., Oudinet, C., Pytowski, L., Bérard, J. B., Nicolau, E., Thiéry, V., Lanneluc, I., Beaugeard, L., Prunier, G., Da Silva Almeida, J. R.G, Picot, L. (2018). Zeaxanthin from Porphyridium purpureum induces apoptosis in human melanoma cells expressing the oncogenic BRAF V600E mutation and sensitizes them to the BRAF inhibitor vemurafenib. Brazilian Journal of Pharmacognosy, 28(4), 457–467. doi: https://doi.org/10.1016/j.bjp.2018.05.009.
  147. 147.
    Barton-Duell, P. (1995). The role of dietary antioxidants in prevention of artherosclerosis. Endocrinologist, 5(5), 347–356.CrossRefGoogle Scholar
  148. 148.
    Giovannucci, E. (1999). Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. Journal of the National Cancer Institute, 91(4), 317–331.  https://doi.org/10.1093/jnci/91.4.317.CrossRefPubMedGoogle Scholar
  149. 149.
    Wolf, F., Nonomura, A., & Bassham, J. (1985). Growth and branched hydrocarbon production in a strain of Botryococcus braunii Chlorophyta. Journal of Phycology, 21, 388–396.CrossRefGoogle Scholar
  150. 150.
    Metzger, P., & Largeau, C. (2005). Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Applied Microbiology and Biotechnology, 66(5), 486–496.  https://doi.org/10.1007/s00253-004-1779-z.CrossRefPubMedGoogle Scholar
  151. 151.
    Bwapwa, J. K., Anandraj, A., & Trois, C. (2017). Possibilities for conversion of microalgae oil into aviation fuel: a review. Renewable and Sustainable Energy Reviews, 80, 1345–1354.  https://doi.org/10.1016/j.rser.2017.05.224.CrossRefGoogle Scholar
  152. 152.
    Matsuura, H., Watanabe, M. M., & Kaya, K. (2012). Echinenone production of a dark red-coloured strain of Botryococcus braunii. Journal of Applied Phycology, 24(4), 973–977.  https://doi.org/10.1007/s10811-011-9719-7.CrossRefGoogle Scholar
  153. 153.
    Abidov, M., Ramazanov, Z., Seifulla, R., & Grachev, S. (2010). The effects of Xanthigen™ in the weight management of obese premenopausal women with non-alcoholic fatty liver disease and normal liver fat. Diabetes, Obesity and Metabolism, 12(1), 72–81.  https://doi.org/10.1111/j.1463-1326.2009.01132.x.CrossRefPubMedGoogle Scholar
  154. 154.
    Wang, S., Verma, S. K., Hakeem Said, I., Thomsen, L., Ullrich, M. S., & Kuhnert, N. (2018). Changes in the fucoxanthin production and protein profiles in Cylindrotheca closterium in response to blue light-emitting diode light. Microbial Cell Factories, 17(1), 1–13.  https://doi.org/10.1186/s12934-018-0957-0.CrossRefGoogle Scholar
  155. 155.
    Wang, H., Zhang, Y., Chen, L., Cheng, W., & Liu, T. (2018). Combined production of fucoxanthin and EPA from two diatom strains Phaeodactylum tricornutum and Cylindrotheca fusiformis cultures. Bioprocess and Biosystems Engineering, 41(7), 1061–1071.  https://doi.org/10.1007/s00449-018-1935-y.CrossRefPubMedGoogle Scholar
  156. 156.
    Xia, S., Wang, K., Wan, L., Li, A., Hu, Q., & Zhang, C. (2013). Production, characterization, and antioxidant activity of fucoxanthin from the marine diatom Odontella aurita. Marine Drugs, 11(7), 2667–2681.  https://doi.org/10.3390/md11072667.CrossRefPubMedPubMedCentralGoogle Scholar
  157. 157.
    Ugwu, C. U., Aoyagi, H., & Uchiyama, H. (2008). Photobioreactors for mass cultivation of algae. Bioresource Technology, 99(10), 4021–4028.  https://doi.org/10.1016/j.biortech.2007.01.046.CrossRefPubMedGoogle Scholar
  158. 158.
    Carvalho, J. C. M., Matsudo, M. C., Bezerra, R. P., Ferreira-Camargo, L. S., & Sato, S. (2014). Microalgae bioreactors. In R. Bajpai, A. Prokop, & M. Zappi (Eds.), Algal biorefineries (pp. 83–126). Netherlands: Springer.CrossRefGoogle Scholar
  159. 159.
    Borowitzka, M. (1999). Commercial production of microalgae: pond, tanks, tubes and fermenters. Journal of Biotechnology, 70(1–3), 313–321.CrossRefGoogle Scholar
  160. 160.
    Brennan, L., & Owende, P. (2010). Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renewable and Sustainable Energy Reviews, 14(2), 557–577.  https://doi.org/10.1016/j.rser.2009.10.009.CrossRefGoogle Scholar
  161. 161.
    Ferreira, L. S., Rodrigues, M. S., Converti, A., Sato, S., & Carvalho, J. C. M. (2012). Arthrospira (Spirulina) platensis cultivation in tubular photobioreactor: use of no-cost CO2 from ethanol fermentation. Applied Energy, 92, 379–385.  https://doi.org/10.1016/j.apenergy.2011.11.019.CrossRefGoogle Scholar
  162. 162.
    Matsudo, M. C., Bezerra, R. P., Converti, A., Sato, S., & Carvalho, J. C. M. (2011). CO2 from alcoholic fermentation for continuous cultivation of Arthrospira (Spirulina) platensis in tubular photobioreactor using urea as nitrogen source. Biotechnology Progress, 27(3), 650–656.  https://doi.org/10.1002/btpr.581.CrossRefPubMedGoogle Scholar
  163. 163.
    Pérez-Mora, L. S., Matsudo, M. C., Cezare-Gomes, E. A., & Carvalho, J. C. M. (2016). An investigation into producing Botryococcus braunii in a tubular photobioreactor. Journal of Chemical Technology and Biotechnology, 91(12), 3053–3060.  https://doi.org/10.1002/jctb.4934.CrossRefGoogle Scholar
  164. 164.
    Eze, C. N., Ogbonna, J. C., Ogbonna, I. O., & Aoyagi, H. (2017). A novel flat plate air-lift photobioreactor with inclined reflective broth circulation guide for improved biomass and lipid productivity by Desmodesmus subspicatus LC172266. Journal of Applied Phycology, 29(6), 2745–2754.  https://doi.org/10.1007/s10811-017-1153-z.CrossRefGoogle Scholar
  165. 165.
    Liao, Q., Sun, Y., Huang, Y., Xia, A., Fu, Q., & Zhu, X. (2017). Simultaneous enhancement of Chlorella vulgaris growth and lipid accumulation through the synergy effect between light and nitrate in a planar waveguide flat-plate photobioreactor. Bioresource Technology, 243, 528–538.  https://doi.org/10.1016/j.biortech.2017.06.091.CrossRefPubMedGoogle Scholar
  166. 166.
    Gao, B., Chen, A., Zhang, W., Li, A., & Zhang, C. (2017). Co-production of lipids, eicosapentaenoic acid, fucoxanthin, and chrysolaminarin by Phaeodactylum tricornutum cultured in a flat-plate photobioreactor under varying nitrogen conditions. Journal of Ocean University of China, 16(5), 916–924.  https://doi.org/10.1007/s11802-017-3174-2.CrossRefGoogle Scholar
  167. 167.
    Koller, A. P., Löwe, H., Schmid, V., Mundt, S., & Weuster-Botz, D. (2017). Model-supported phototrophic growth studies with Scenedesmus obtusiusculus in a flat-plate photobioreactor. Biotechnology and Bioengineering, 114(2), 308–320.  https://doi.org/10.1002/bit.26072.CrossRefPubMedGoogle Scholar
  168. 168.
    Koller, A. P., Wolf, L., & Weuster-Botz, D. (2017). Reaction engineering analysis of Scenedesmus ovalternus in a flat-plate gas-lift photobioreactor. Bioresource Technology, 225, 165–174.  https://doi.org/10.1016/j.biortech.2016.11.025.CrossRefPubMedGoogle Scholar
  169. 169.
    Hulatt, C. J., Wijffels, R. H., Bolla, S., & Kiron, V. (2017). Production of fatty acids and protein by Nannochloropsis in flat-plate photobioreactors. PLoS One, 12(1), 1–17.  https://doi.org/10.1371/journal.pone.0170440.CrossRefGoogle Scholar
  170. 170.
    López-Rosales, L., García-Camacho, F., Sánchez-Mirón, A., Contreras-Gómez, A., & Molina-Grima, E. (2017). Modeling shear-sensitive dinoflagellate microalgae growth in bubble column photobioreactors. Bioresource Technology, 245(Pt A), 250–257.  https://doi.org/10.1016/j.biortech.2017.08.161.CrossRefPubMedGoogle Scholar
  171. 171.
    Plouviez, M., Shilton, A., Packer, M. A., & Guieysse, B. (2017). N2O emissions during microalgae outdoor cultivation in 50 L column photobioreactors. Algal Research, 26, 348–353.  https://doi.org/10.1016/j.algal.2017.08.008.CrossRefGoogle Scholar
  172. 172.
    Kim, Z. H., Park, Y. S., Ryu, Y. J., & Lee, C. G. (2017). Enhancing biomass and fatty acid productivity of Tetraselmis sp. in bubble column photobioreactors by modifying light quality using light filters. Biotechnology and Bioprocess Engineering, 22(4), 397–404.  https://doi.org/10.1007/s12257-017-0200-6.CrossRefGoogle Scholar
  173. 173.
    Huntley, M. E., Johnson, Z. I., Brown, S. L., Sills, D. L., Gerber, L., Archibald, I., Machesky, S. C., Granados, J., Beal, C., & Greene, C. H. (2015). Demonstrated large-scale production of marine microalgae for fuels and feed. Algal Research, 10, 249–265.  https://doi.org/10.1016/j.algal.2015.04.016.CrossRefGoogle Scholar
  174. 174.
    Cyanotech Corporation. (2018). Cyanotech—astaxanthin process. Retrieved August 22, 2018, from https://www.cyanotech.com/astaxanthin/astaxanthin-process/
  175. 175.
    Fu, W., Paglia, G., Magnúsdóttir, M., Steinarsdóttir, E. A., Gudmundsson, S., Palsson, B. Ó., Andrésson, Ó. S., & Brynjólfsson, S. (2014). Effects of abiotic stressors on lutein production in the green microalga Dunaliella salina. Microbial Cell Factories, 13(1), 3.  https://doi.org/10.1186/1475-2859-13-3.CrossRefPubMedPubMedCentralGoogle Scholar
  176. 176.
    Cuaresma, M., Casal, C., Forján, E., & Vílchez, C. (2011). Productivity and selective accumulation of carotenoids of the novel extremophile microalga Chlamydomonas acidophila grown with different carbon sources in batch systems. Journal of Industrial Microbiology and Biotechnology, 38(1), 167–177.  https://doi.org/10.1007/s10295-010-0841-3.CrossRefPubMedGoogle Scholar
  177. 177.
    Castro-Puyana, M., Pérez-Sánchez, A., Valdés, A., Ibrahim, O. H. M., Suarez-Álvarez, S., Ferragut, J. A., Micol, V., Cifuentes, A., Ibáñez, E., & García-Cañas, V. (2017). Pressurized liquid extraction of Neochloris oleoabundans for the recovery of bioactive carotenoids with anti-proliferative activity against human colon cancer cells. Food Research International, 99(Pt 3), 1048–1055.  https://doi.org/10.1016/j.foodres.2016.05.021.CrossRefPubMedGoogle Scholar
  178. 178.
    Ma, R., Thomas-Hall, S. R., Chua, E. T., Eltanahy, E., Netzel, M. E., Netzel, G., Lu, Y., & Schenk, P. M. (2018). LED power efficiency of biomass, fatty acid, and carotenoid production in Nannochloropsis microalgae. Bioresource Technology, 252(December 2017), 118–126.  https://doi.org/10.1016/j.biortech.2017.12.096.CrossRefPubMedGoogle Scholar
  179. 179.
    Pan-utai, W., Parakulsuksatid, P., & Phomkaivon, N. (2017). Effect of inducing agents on growth and astaxanthin production in Haematococcus pluvialis: organic and inorganic. Biocatalysis and Agricultural Biotechnology, 12, 152–158.  https://doi.org/10.1016/j.bcab.2017.10.004.CrossRefGoogle Scholar
  180. 180.
    Dayananda, C., & Kumudha, A. (2010). Isolation, characterization and outdoor cultivation of green microalgae Botryococcus sp. Scientific Research and Essays, 5(17), 2497–2505 Retrieved from http://www.academicjournals.org/sre/pdf/pdf2010/4Sep/Dayanandae al.pdf.Google Scholar
  181. 181.
    Zhu, L. (2015). Microalgal culture strategies for biofuel production: a review. Biofuels, Bioproducts and Biorefining, 9(6), 801–814.  https://doi.org/10.1002/bbb.1576.CrossRefGoogle Scholar
  182. 182.
    García-cañedo, J. C., Cristiani-urbina, E., Flores-ortiz, C. M., Ponce-noyola, T., Esparza-garcía, F., & Cañizares-villanueva, R. O. (2016). Batch and fed-batch culture of Scenedesmus incrassatulus: effect over biomass, carotenoid profile and concentration, photosynthetic efficiency and non-photochemical quenching. Algal, 13, 41–52.  https://doi.org/10.1016/j.algal.2015.11.013.CrossRefGoogle Scholar
  183. 183.
    Sun, N., Wang, Y., Li, Y. T., Huang, J. C., & Chen, F. (2008). Sugar-based growth, astaxanthin accumulation and carotenogenic transcription of heterotrophic Chlorella zofingiensis (Chlorophyta). Process Biochemistry, 43(11), 1288–1292.  https://doi.org/10.1016/j.procbio.2008.07.014.CrossRefGoogle Scholar
  184. 184.
    Chen, C. Y., Lu, I. C., Nagarajan, D., Chang, C. H., Ng, I. S., Lee, D. J., & Chang, J. S. (2018). A highly efficient two-stage cultivation strategy for lutein production using heterotrophic culture of Chlorella sorokiniana MB-1-M12. Bioresource Technology, 253, 141–147.  https://doi.org/10.1016/j.biortech.2018.01.027.CrossRefPubMedGoogle Scholar
  185. 185.
    Park, J. C., Choi, S. P., Hong, M. E., & Sim, S. J. (2014). Enhanced astaxanthin production from microalga, Haematococcus pluvialis by two-stage perfusion culture with stepwise light irradiation. Bioprocess and Biosystems Engineering, 37(10), 2039–2047.  https://doi.org/10.1007/s00449-014-1180-y.CrossRefPubMedGoogle Scholar
  186. 186.
    Liu, J., Mao, X., Zhou, W., & Guarnieri, M. T. (2016). Simultaneous production of triacylglycerol and high-value carotenoids by the astaxanthin-producing oleaginous green microalga Chlorella zofingiensis. Bioresource Technology, 214, 319–327.  https://doi.org/10.1016/j.biortech.2016.04.112.CrossRefPubMedGoogle Scholar
  187. 187.
    Dineshkumar, R., Subramanian, G., Dash, S. K., & Sen, R. (2016). Development of an optimal light-feeding strategy coupled with semi-continuous reactor operation for simultaneous improvement of microalgal photosynthetic efficiency, lutein production and CO2 sequestration. Biochemical Engineering Journal, 113, 47–56.  https://doi.org/10.1016/j.bej.2016.05.011.CrossRefGoogle Scholar
  188. 188.
    Prieto, A., Pedro Cañavate, J., & García-González, M. (2011). Assessment of carotenoid production by Dunaliella salina in different culture systems and operation regimes. Journal of Biotechnology, 151(2), 180–185.  https://doi.org/10.1016/j.jbiotec.2010.11.011.CrossRefPubMedGoogle Scholar
  189. 189.
    García-González, M., Moreno, J., Manzano, J. C., Florencio, F. J., & Guerrero, M. G. (2005). Production of Dunaliella salina biomass rich in 9-cis-β-carotene and lutein in a closed tubular photobioreactor. Journal of Biotechnology, 115(1), 81–90.  https://doi.org/10.1016/j.jbiotec.2004.07.010.CrossRefPubMedGoogle Scholar
  190. 190.
    Chaumont Daniel, C. T. (1995). Carotenoid content in growing cells of Haematococcus pluvialis during a sunlight cycle. Journal of Applied Phycology, 7.6(1995), 529–537 APA, (1993), 529–537.CrossRefGoogle Scholar
  191. 191.
    Barbosa, M. J., Zijffers, J. W., Nisworo, A., Vaes, W., Van Schoonhoven, J., & Wijffels, R. H. (2005). Optimization of biomass, vitamins, and carotenoid yield on light energy in a flat-panel reactor using the A-stat technique. Biotechnology and Bioengineering, 89(2), 233–242.  https://doi.org/10.1002/bit.20346.CrossRefPubMedGoogle Scholar
  192. 192.
    Cerón, M. C., García-Malea, M. C., Rivas, J., Acien, F. G., Fernandez, J. M., Del Río, E., Guerrero, M. G., & Molina, E. (2007). Antioxidant activity of Haematococcus pluvialis cells grown in continuous culture as a function of their carotenoid and fatty acid content. Applied Microbiology and Biotechnology, 74(5), 1112–1119.  https://doi.org/10.1007/s00253-006-0743-5.CrossRefPubMedGoogle Scholar
  193. 193.
    Wang, S. K., Stiles, A. R., Guo, C., & Liu, C. Z. (2014). Microalgae cultivation in photobioreactors: an overview of light characteristics. Engineering in Life Sciences, 14(6), 550–559.  https://doi.org/10.1002/elsc.201300170.CrossRefGoogle Scholar
  194. 194.
    Carvalho, A. P., Silva, S. O., Baptista, J. M., & Malcata, F. X. (2011). Light requirements in microalgal photobioreactors: an overview of biophotonic aspects. Applied Microbiology and Biotechnology, 89(5), 1275–1288.  https://doi.org/10.1007/s00253-010-3047-8.CrossRefPubMedGoogle Scholar
  195. 195.
    Blanken, W., Cuaresma, M., Wijffels, R. H., & Janssen, M. (2013). Cultivation of microalgae on artificial light comes at a cost. Algal Research, 2(4), 333–340.  https://doi.org/10.1016/j.algal.2013.09.004.CrossRefGoogle Scholar
  196. 196.
    Matthijs, H. C. P., Balke, H., Van Hes, U. M., Kroon, B. M. A., Mur, L. R., & Binot, R. A. (1996). Application of light-emitting diodes in bioreactors: flashing light effects and energy economy in algal culture (Chlorella pyrenoidosa). Biotechnology and Bioengineering, 50(1), 98–107.  https://doi.org/10.1002/(SICI)1097-0290(19960405)50:1<98::AID-BIT11>3.0.CO;2-3.CrossRefPubMedGoogle Scholar
  197. 197.
    Schulze, P. S. C., Barreira, L. A., Pereira, H. G. C., Perales, J. A., & Varela, J. C. S. (2014). Light emitting diodes (LEDs) applied to microalgal production. Trends in Biotechnology, 32(8), 422–430.  https://doi.org/10.1016/j.tibtech.2014.06.001.CrossRefPubMedGoogle Scholar
  198. 198.
    Kula, M., Rys, M., Mozdzeń, K., & Skoczowski, A. (2014). Metabolic activity, the chemical composition of biomass and photosynthetic activity of Chlorella vulgaris under different light spectra in photobioreactors. Engineering in Life Sciences, 14(1), 57–67.  https://doi.org/10.1002/elsc.201200184.CrossRefGoogle Scholar
  199. 199.
    Fu, W., Guomundsson, Ó., Paglia, G., Herjólfsson, G., Andrésson, Ó. S., Palsson, B. O., & Brynjólfsson, S. (2013). Enhancement of carotenoid biosynthesis in the green microalga Dunaliella salina with light-emitting diodes and adaptive laboratory evolution. Applied Microbiology and Biotechnology, 97(6), 2395–2403.  https://doi.org/10.1007/s00253-012-4502-5.CrossRefPubMedGoogle Scholar
  200. 200.
    Katsuda, T., Lababpour, A., Shimahara, K., & Katoh, S. (2004). Astaxanthin production by Haematococcus pluvialis under illumination with LEDs. Enzyme and Microbial Technology, 35(1), 81–86.  https://doi.org/10.1016/j.enzmictec.2004.03.016.CrossRefGoogle Scholar
  201. 201.
    Baba, M., Kikuta, F., Suzuki, I., Watanabe, M. M., & Shiraiwa, Y. (2012). Wavelength specificity of growth, photosynthesis, and hydrocarbon production in the oil-producing green alga Botryococcus braunii. Bioresource Technology, 109, 266–270.  https://doi.org/10.1016/j.biortech.2011.05.059.CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Eleane A. Cezare-Gomes
    • 1
  • Lauris del Carmen Mejia-da-Silva
    • 1
  • Lina S. Pérez-Mora
    • 1
  • Marcelo C. Matsudo
    • 2
  • Lívia S. Ferreira-Camargo
    • 3
  • Anil Kumar Singh
    • 4
  • João Carlos Monteiro de Carvalho
    • 1
    Email author return OK on get
  1. 1.Department of Biochemical and Pharmaceutical TechnologyUniversity of São PauloSão PauloBrazil
  2. 2.Institute of Natural ResourcesFederal University of ItajubáItajubáBrazil
  3. 3.Center of Natural and Human SciencesFederal University of ABCSanto AndréBrazil
  4. 4.Department of PharmacyUniversity of São PauloSão PauloBrazil

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