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Outdoor cultivation of microalgae for carotenoid production: current state and perspectives

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Abstract

Microalgae are a major natural source for a vast array of valuable compounds, including a diversity of pigments, for which these photosynthetic microorganisms represent an almost exclusive biological resource. Yellow, orange, and red carotenoids have an industrial use in food products and cosmetics as vitamin supplements and health food products and as feed additives for poultry, livestock, fish, and crustaceans. The growing worldwide market value of carotenoids is projected to reach over US$1,000 million by the end of the decade. The nutraceutical boom has also integrated carotenoids mainly on the claim of their proven antioxidant properties. Recently established benefits in human health open new uses for some carotenoids, especially lutein, an effective agent for the prevention and treatment of a variety of degenerative diseases. Consumers’ demand for natural products favors development of pigments from biological sources, thus increasing opportunities for microalgae. The biotechnology of microalgae has gained considerable progress and relevance in recent decades, with carotenoid production representing one of its most successful domains. In this paper, we review the most relevant features of microalgal biotechnology related to the production of different carotenoids outdoors, with a main focus on β-carotene from Dunaliella, astaxanthin from Haematococcus, and lutein from chlorophycean strains. We compare the current state of the corresponding production technologies, based on either open-pond systems or closed photobioreactors. The potential of scientific and technological advances for improvements in yield and reduction in production costs for carotenoids from microalgae is also discussed.

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References

  • Alves-Rodrigues A, Shao A (2004) The science behind lutein. Toxicol Lett 150:57–83

    CAS  PubMed  Google Scholar 

  • Astorg P (1997) Food carotenoids and cancer prevention: an overview of current research. Trends Food Sci Technol 8:406–413

    CAS  Google Scholar 

  • Ben-Amotz A (1995) New mode of Dunaliella biotechnology: two-phase growth for β-carotene production. J Appl Phycol 7:65–68

    CAS  Google Scholar 

  • Ben-Amotz A (1999) Dunaliella β-carotene: from science to commerce. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Kluwer, Netherlands, pp 401–410

    Google Scholar 

  • Ben-Amotz A (2004) Industrial production of microalgal cell-mass and secondary products—major industrial species. Dunaliella. In: Richmond A (ed) Handbook of microalgal culture. Biotechnology and applied phycology. Blackwell Science, Oxford, UK, pp 273–280

    Google Scholar 

  • Ben-Amotz A, Avron M (1990) The biotechnology of cultivating the halotolerant alga Dunaliella. Trends Biotechnol 8:121–125

    CAS  Google Scholar 

  • Ben-Amotz A, Shaish A (1992) β-carotene biosynthesis. In: Avron M, Ben-Amotz A (eds) Dunaliella: physiology, biochemistry and biotechnology. CRC Press, Boca Raton, Florida, pp 206–216

    Google Scholar 

  • Bhosale P, Bernstein PS (2005) Microbial xanthophylls. Appl Microbiol Biotechnol 68:445–455

    CAS  PubMed  Google Scholar 

  • Blanco AM, Moreno J, Del Campo JA, Rivas J, Guerrero MG (2007) Outdoor cultivation of lutein-rich cells of Muriellopsis sp. in open ponds. Appl Microbiol Biotechnol 73:1259–1266

    CAS  PubMed  Google Scholar 

  • Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 7:3–15

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Borowitzka MA, Borowitzka LJ (1988) Dunaliella. In: Borowitzka MA, Borowitzka LJ (eds) Micro-algal biotechnology. Cambridge University Press, Cambridge, UK, pp 27–58

    Google Scholar 

  • Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117

    CAS  Google Scholar 

  • Boussiba S, Vonshak A (1991) Astaxanthin accumulation in the green alga Haematococcus pluvialis. Plant Cell Physiol 32:1077–1082

    CAS  Google Scholar 

  • Cerón-García MC, García-Malea MC, Rivas J, Acien FG, Fernández-Sevilla JM, del Rio E, Guerrero MG, Molina-Grima E (2007) Antioxidant activity of Haematococcuspluvialis cells grown in continuous culture an a function of their carotenoid and fatty acid content. Appl Microbiol Biotechnol (in press). DOI https://doi.org/10.1007/s00253-006-0743-5

    PubMed  Google Scholar 

  • Chaumont D, Thépenier C (1995) Carotenoid content in growing cells of Haematococcus pluvialis during a sunlight cycle. J Appl Phycol 7:529–537

    CAS  Google Scholar 

  • Cysewski GR, Todd Lorenz R (2004) Industrial production of microalgal cell-mass and secondary products—species of high potential. Haematococcus. In: Richmond A (ed) Handbook of microalgal culture. Biotechnology and applied phycology. Blackwell Science, Oxford, UK, pp 281–288

    Google Scholar 

  • Del Campo JA, Moreno J, Rodríguez H, Vargas MA, Rivas J, Guerrero MG (2000) Carotenoid content of chlorophycean microalgae. Factors determining lutein accumulation in Muriellopsis sp. (Chlorophyta). J Biotechnol 76:51–59

    PubMed  Google Scholar 

  • Del Campo JA, Rodríguez H, Moreno J, Vargas MA, Rivas J, Guerrero MG (2001) Lutein production by Muriellopsis sp. in an outdoor tubular photobioreactor. J Biotechnol 81:289–295

    Google Scholar 

  • Del Campo JA, Rodríguez H, Moreno J, Vargas MA, Rivas J, Guerrero MG (2004) Accumulation of astaxanthin and lutein in Chlorella zofingiensis (Chlorophyta). Appl Microbiol Biotechnol 64:848–854

    PubMed  Google Scholar 

  • Del Río E, Acién FG, García-Malea MC, Rivas J, Molina-Grima E, Guerrero MG (2005a) Efficient one-step production of astaxanthin by the microalga Haematococcus pluvialis in continuous culture. J Biotechnol 91:808–815

    Google Scholar 

  • Del Río E, Blanco AM, Rivas J, Guerrero MG (2005b) Performance of maintained astaxanthin generation by Haematococcus pluvialis in a one-step continuous system. In: Abstracts 10th international conference on applied phycology, Kunming, China, pp 111–112

  • Demming-Adams B, Adams WW III (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153

    Google Scholar 

  • Dunahay TG (1996) Manipulation of microalgal lipid production using genetic engineering. Appl Biochem Biotechnol 57–58:223–231

    Google Scholar 

  • Dwyer JH, Navab M, Dwyer KM, Hassan K, Sun P, Shircore A, Hama-Levy S, Hough G, Wang X, Drake T, Merz NB, Fogelman AM (2001) Oxygenated carotenoid lutein and the progression of early atherosclerosis. The Los Angeles atherosclerosis study. Circulation 103:2922–2927

    CAS  PubMed  Google Scholar 

  • Edge R, McGarvey DJ, Truscott TG (1997) The carotenoids as antioxidants—a review. J Photochem Photobiol B Biol 41:189–200

    CAS  Google Scholar 

  • Eom H, Lee C-G, Jin ES (2006) Gene expression profile analysis in astaxanthin-induced Haematococcus pluvialis using a cDNA microarray. Planta 223:1231–1242

    CAS  PubMed  Google Scholar 

  • Fábregas J, Otero A, Maseda A, Domínguez A (2001) Two-stage cultures for the production of astaxanthin from Haematococcus pluvialis. J Biotechnol 89:65–71

    PubMed  Google Scholar 

  • Fábregas J, Domínguez A, Maseda A, Otero A (2003) Interactions between irradiance and nutrient availability during astaxanthin accumulation and degradation in Haematococcus pluvialis. Appl Microbiol Biotechnol 61:545–551

    PubMed  Google Scholar 

  • García-González M, Moreno J, Cañavate JP, Anguis V, Prieto A, Manzano C, Florencio FJ, Guerrero MG (2003) Conditions for open-air outdoor culture of Dunaliella salina in Southern Spain. J Appl Phycol 15:177–184

    Google Scholar 

  • García-González M, Moreno J, Manzano C, Florencio FJ, Guerrero MG (2005) Production of Dunaliella salina biomass rich in 9-cis β-carotene and lutein in a closed tubular photobioreactor. J Biotechnol 115:81–90

    PubMed  Google Scholar 

  • García-Malea MC, Del Río E, Casas López JL, Acién Fernández FG, Fernández Sevilla JM, Rivas J, Guerrero MG, Molina Grima E (2006) Comparative analysis of the outdoor culture of Haematococcus pluvialis in tubular and bubble column photobioreactors. J Biotechnol 123:329–342

    Google Scholar 

  • George SB, Lawrence JM, Lawrence AL, Smiley J, Plank L (2001) Carotenoids in the adult diet enhance egg and juvenile production in the sea urchin Lytechinus variegatus. Aquaculture 199:353–369

    CAS  Google Scholar 

  • Granado F, Olmedilla B, Blanco I (2003) Nutritional and clinical relevance of lutein in human health. Brit J Nutr 90:487–502

    CAS  PubMed  Google Scholar 

  • Grossman AR, Lohr M, Im CS (2004) Chlamydomonas reinhardtii in the landscape of pigments. Annu Rev Genet 38:119–173

    CAS  PubMed  Google Scholar 

  • Gudin C (2003) Une historie naturelle de la séduction. Éditions du Seuil, Paris, France

    Google Scholar 

  • Gudin C, Chaumont D (1980) A biotechnology of photosynthetic cells based on the use of solar energy. Biochem Soc Trans 8:481–482

    CAS  PubMed  Google Scholar 

  • Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 21:210–216

    CAS  PubMed  Google Scholar 

  • Guerrero MG, Del Río E, Acién FG, García-Malea MC, Rivas J, Molina-Grima E (2006) Influence of nitrogen supply and irradiance on astaxanthin accumulation by Haematococcus pluvialis in continuous culture. In: Abstracts of 2nd FEMS congress of European microbiologists. Integrating microbial knowledge into human life, Madrid, p 118

  • Harker M, Tsavalos AJ, Young AJ (1995) Use of response surface methodology to optimise carotenogenesis in the microalga Haematococcus pluvialis. J Appl Phycol 7:399–406

    Google Scholar 

  • Hejazi MA, Lamarliere C, Rocha JMS, Vermüe M, Tramper J, Wijffels RH (2002) Selective extraction of carotenoids from the microalga Dunaliella salina with retention of viability. Biotechnol Bioeng 79:30–36

    Google Scholar 

  • Hejazi MA, Anddrysiewicz E, Tramper J, Wijffels RH (2003) Effect of mixing rate on β-carotene production and extraction by Dunaliella salina in two-phase bioreactor. Biotechnol Bioeng 84:591–596

    CAS  PubMed  Google Scholar 

  • Higuera-Ciapara I, Félix-Valenzuela L, Goycoolea FM (2006) Astaxanthin: a review of its chemistry and applications. Crit Rev Food Sci Nutr 46:185–196

    CAS  PubMed  Google Scholar 

  • Hussein G, Sankawa U, Goto H, Matsumoto K, Watanabe H (2006) Astaxanthin, a carotenoid with potential in human health and nutrition. J Nat Prod 69:443–449

    CAS  PubMed  Google Scholar 

  • Johnson EA, Schroeder WA (1995) Microbial carotenoids. Adv Biochem Eng Biotechnol 53:119–178

    Google Scholar 

  • Kang CD, Lee JS, Park TH, Sim SJ (2005) Comparison of heterotrophic and photoautotrophic induction on astaxanthin production by Haematococcus pluvialis. Appl Microbiol Biotechnol 68:237–241

    CAS  PubMed  Google Scholar 

  • Kim HW, Chew BP, Wong TS, Park JS, Weng BBC, Byrne KM, Hayek MG, Reinhart GA (2000a) Modulation of humoral and cell-mediated immune responses by dietary lutein in cats. Vet Immunol Immunopathol 73:331–341

    CAS  PubMed  Google Scholar 

  • Kim HW, Chew BP, Wong TS, Park JS, Weng BBC, Byrne KM, Hayek MG, Reinhart GA (2000b) Dietary lutein stimulates immune response in the canine. Vet Immunol Immunopathol 74:315–327

    CAS  PubMed  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

    CAS  Google Scholar 

  • Kobayashi M, Kakizono T, Nagai S (1992a) Effect of carbon/nitrogen (C/N) ratio on encystment accompanied with astaxanthin formation in a green alga, Haematococcus pluvialis. J Ferment Bioeng 74:403–405

    Google Scholar 

  • Kobayashi M, Kakizono T, Nishio N, Nagai S (1992b) Effects of light intensity, light quality, and illumination cycle on astaxanthin formation in a green alga, Haematococcus pluvialis. J Ferment Bioeng 74:61–63

    CAS  Google Scholar 

  • Koh HH, Murray IJ, Nolan D, Carden D, Feather J, Beatty S (2004) Plasma and macular responses to lutein supplement in subjects with and without age-related maculopathy: a pilot study. Exp Eye Res 79:21–27

    CAS  PubMed  Google Scholar 

  • Krinsky NI, Johnson EJ (2005) Carotenoid actions and their relation to health and disease. Mol Aspects Med 26:459–516

    CAS  PubMed  Google Scholar 

  • Krinsky NI, Landrum JT, Bone RA (2003) Biological mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr 23:171–201

    CAS  PubMed  Google Scholar 

  • Lee YK, Ding SY (1995) Effect of dissolved oxygen partial pressure on the accumulation of astaxanthin in chemostat cultures of Haematococcus lacustris (Chlorophyta). J Phycol 31:922–924

    CAS  Google Scholar 

  • Lee YK, Soh CW (1991) Accumulation of astaxanthin in Haematococcus lacustris (Chlorophyta). J Phycol 27:575–577

    CAS  Google Scholar 

  • León-Bañares R, González-Ballester D, Galván A, Fernández E (2004) Transgenic microalgae as green cell-factories. Trends Biotechnol 22:45–52

    PubMed  Google Scholar 

  • Mares-Perlman JA, Millen AE, Ficek TL, Hankinson SE (2002) The body of evidence to support a protective role for lutein and zeaxanthin in delaying chronic disease. Overview. J Nutr 132:5185–5245

    Google Scholar 

  • Margalith PZ (1999) Production of ketocarotenoids by microalgae. Appl Microbiol Biotechnol 51:431–438

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mendes-Pinto MM, Raposo MFJ, Bowen J, Young AJ, Morais R (2001) Evaluation of different cell disruption processes on encysted cells of Haematococcus pluvialis: effects on astaxanthin recovery and implications on bio-availability. J Appl Phycol 13:19–24

    Google Scholar 

  • Molina-Grima E, Acién Fernández FG, García Camacho F, Chisti Y (1999) Photobioreactors: light regime, mass transfer and scaleup. J Biotechnol 70:231–247

    CAS  Google Scholar 

  • Molina-Grima E, Acién Fernández FG, Robles Medina A (2004) Downstream processing of cell-mass and products. In: Richmond A (ed) Handbook of microalgal culture. Biotechnology and applied phycology. Blackwell Science, Oxford, UK, pp 215–251

    Google Scholar 

  • Negro JJ, Garrido-Fernández J (2000) Astaxanthin is the major carotenoid in tissues of white storks (Ciconia ciconia) feeding on introduced crayfish (Procambarus clarkii). Comp Biochem Physiol Part B Biochem Mol Biol 126:347–352

    CAS  Google Scholar 

  • Ninet L, Renault J (1979) In: Peppler HJ, Perlman D (eds) Microbiol technology, 2nd edn. Academic, New York, pp 529–530

    Google Scholar 

  • Olaizola M (2000) Commercial production of astaxanthin from Haematococus pluvialis using 25,000-liter outdoor photobioreactor. J Appl Phycol 12:499–506

    CAS  Google Scholar 

  • Olaizola M, Huntley ME (2003) Recent advances in commercial production of astaxanthin from microalgae. In: Fingerman M, Nagabhushanam R (eds) Biomaterials and bioprocessing. Enfield Science Publishers, pp 143–164

  • Olmedilla B, Granado F, Blanco I, Vaquero M (2003) Lutein, but not α-tocopherol, supplementation improves visual function in patients with age-related cataracts: a 2-y double-blind, placebo-controlled pilot study. Nutrition 19:21–24

    CAS  PubMed  Google Scholar 

  • Orosa M, Valero JF, Herrero C, Abalde J (2001) Comparison of the accumulation of astaxanthin in Haematococcus and other green microalgae under N-starvation and high light conditions. Biotechnol Lett 23:1079–1085

    CAS  Google Scholar 

  • Orosa M, Franqueira D, Cid A, Abalde J (2005) Analysis and enhancement of astaxanthin accumulation in Haematococcus pluvialis. Bioresour Technol 96:373–378

    CAS  PubMed  Google Scholar 

  • Piccaglia R, Marotti M, Grandi S (1998) Lutein and lutein ester content in different types of Tagetes patula and T. erecta. Ind Crops Prod 8:45–51

    CAS  Google Scholar 

  • Pulz O (2001) Photobioreactors: production systems of phototrophic microorganisms. Appl Microbiol Biotechnol 57:287–293

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Richmond A (2004) Handbook of microalgal culture. Biotechnology and applied phycology. Blackwell Science, Oxford, UK

    Google Scholar 

  • Salter GJ, Kell DB (1995) Solvent selection for whole cell biotransformation in organic media. Crit Rev Biotechnol 15:139–177

    CAS  PubMed  Google Scholar 

  • Sandmann G (2001) Genetic manipulation of carotenoid biosynthesis: strategies, problems and achievements. Trends Plant Sci 6:14–17

    CAS  PubMed  Google Scholar 

  • Sansawa H, Endo H (2004) Production of intracellular phytochemicals in Chlorella under heterotrophic conditions. J Biosci Bioeng 98:437–444

    CAS  PubMed  Google Scholar 

  • Shi X, Zhengyun W, Chen F (2006) Kinetic model of lutein production by heterotrophic Chlorella at various pH and temperature. Mol Nutr Food Res 50:763–768

    CAS  PubMed  Google Scholar 

  • Steinbrenner J, Sandmann G (2006) Transformation of the green alga Haematococcus pluvialis with a phytoene desaturase for accelerated astaxanthin biosynthesis. Appl Environ Microbiol 72:7477–7484

    CAS  PubMed  PubMed Central  Google Scholar 

  • Todd Lorenz R, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167

    Google Scholar 

  • Tredici M (2004) Mass production of microalgae: photobioreactors. In: Richmond A (ed) Handbook of microalgal culture. Blackwell Science, Oxford, UK, pp 178–214

    Google Scholar 

  • Walker TL, Purton S, Becker DK, Collet C (2005) Microalgae as bioreactors. Plant Cell Rep 24:629–641

    CAS  PubMed  Google Scholar 

  • Wang SB, Hu Q, Sommerfeld M, Chen F (2004) Cell wall proteomics of the green alga Haematococcus pluvialis (Chlorophyceae). Proteomics 4:692–708

    CAS  PubMed  Google Scholar 

  • Weissman JC, Goebel RP, Benemann JR (1988) Photobioreactor design: mixing, carbon utilization, and oxygen accumulation. Biotechnol Bioeng 31:336–344

    CAS  PubMed  Google Scholar 

  • Whitehead AJ, Mares JA, Danis RP (2006) Macular pigment: a review of current knowledge. Arch Ophtalmol 124:1038–1045

    CAS  Google Scholar 

  • Zaslavskaia LA, Lippmeier JC, Shih C, Erhardt D, Grossman AR, Apt K (2001) Trophic conversion of an obligate photoautotrophic organism through metabolic engineering. Science 292:2073–2075

    CAS  PubMed  Google Scholar 

  • Zhang DH, Lee YK (1997) Enhanced accumulation of secondary carotenoids in a mutant of the green alga, Chlorococcum sp. J Appl Phycol 9:459–463

    CAS  Google Scholar 

  • Zlotnik IS, Sukenik A, Dubinsky Z (1993) Physiological and photosynthetic changes during the formation of red aplanospores in the chlorophyte Haematococcus pluvialis. J Phycol 29:463–469

    Google Scholar 

  • Zorn H, Breithaupt DE, Takenberg M, Schwack W, Berger RG (2003) Enzymatic hydrolysis of carotenoid esters of marigold flowers (Tagetes erecta L.) and red paprika (Capsicum annuum L.) by commercial lipases and Pleorotus sapidus extracellular lipase. Enzyme Microb Technol 32:623–628

    CAS  Google Scholar 

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Acknowledgment

The authors thank Drs. Fernández Sevilla, Acién Fernández, and Molina Grima—from the Department of Chemical Engineering, University of Almería, Spain—for providing unpublished data on lutein content and productivity of Scenedesmus almeriensis, as well as the photobioreactor photograph. Work from the authors’ laboratory was supported by grants PPQ2001-3832-C02-01 and BIO2004-05834-C02-02, from Plan Nacional, Ministerio de Educación y Ciencia (cofinanced with FEDER funds from EU), IFAPA (CO3-125), and Plan Andaluz de Investigación (group no. CVI131), Spain.

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  1. Instituto de Bioquímica Vegetal y Fotosíntesis, Universidad de Sevilla-Consejo Superior de Investigaciones Científicas, Avda. Américo Vespucio 49, Sevilla, 41092, Spain

    José A. Del Campo, Mercedes García-González & Miguel G. Guerrero

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  1. José A. Del Campo
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Correspondence to Miguel G. Guerrero.

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Del Campo, J.A., García-González, M. & Guerrero, M.G. Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 74, 1163–1174 (2007). https://doi.org/10.1007/s00253-007-0844-9

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