Abstract
The growth performance of the chlorophycean microalga Muriellopsis sp. outdoors in open tanks agitated with a paddlewheel and its ability to accumulate carotenoids have been evaluated throughout the year. The cells grown in the open system had free lutein as the main carotenoid, with violaxanthin, β-carotene, and neoxanthin also present. Lutein content of the dry biomass ranged from 0.4 to 0.6%, depending on the growth and environmental conditions. In addition, the biomass of Muriellopsis sp. had a high content in both protein and lipids with about half of the fatty acids being of the polyunsaturated type, with α-linolenic acid accounting for almost 30% of the total fatty acids. The effect of determinant parameters on the performance of the cultures in open tanks was evaluated. Operating conditions that allow the maintenance of productive cultures were established under semicontinuous regime for 9 months throughout the year. Biomass and lutein yields in the open system were not far from those in closed tubular photobioreactors, and reached productivity values of 20 g dry biomass, containing around 100 mg lutein m−2 day−1 in summer. The outdoor culture of Muriellopsis sp. in open ponds thus represents a real alternative to established systems for the production of lutein.
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References
Alves-Rodrigues A, Shao A (2004) The science behind lutein. Toxicol Lett 150:57–83
Apt K, Behrens P (1999) Commercial developments in microalgal biotechnology. J Phycol 35:215–226
Arnon DI, McSwain BD, Tsujimoto HY, Wada K (1974) Photochemical activity and components of membrane preparations from blue-green algae. I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin. Biochim Biophys Acta 357:231–245
Astorg P (1997) Food carotenoids and cancer prevention: an overview of current research. Trends Food Sci Technol 8:406–413
Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127
Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 7:3–15
Borowitzka MA (1999) Commercial production of microalgae: ponds, tanks, tubes and fermenters. J Biotechnol 70:313–321
Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for marineculture. Aquaculture 151:315–331
Chew BP (1996) Importance of antioxidant vitamins in immunity and health in animals. Anim Feed Sci Technol 59:103–114
De Pauw N, Persoone G (1988) Micro-algae for aquaculture. In: Borowitzka MA, Borowitzka LJ (eds) Micro-algal biotechnology. Cambridge University Press, Cambridge, UK, pp 197–221
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
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
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(6):848–854
Demming-Adams B, Adams WW III (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Dunstan GA, Volkman JK, Jeffrey SW, Barrett SM (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 2. Lipid classes and fatty acid. J Exp Mar Biol Ecol 161:115–134
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
Goldman JC (1979) Outdoor algal mass cultures. II. Photosynthetic field limitations. Water Res 13:119–160
Granado F, Olmedilla B, Blanco I (2003) Nutritional and clinical relevance of lutein in human health. Br J Nutr 90:487–502
Herbert D, Phipps PJ, Strange RE (1971) Chemicals analysis of microbial cells. In: Norris JR, Ribbons DW (eds) Methods in microbiology, vol 5B. Academic, London, pp 209–344
Jiménez C, Cossío BR, Labella D, Niell FX (2003) The feasibility of industrial production of Spirulina (Arthrospira) in southern Spain. Aquaculture 217:179–190
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
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
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
Krinsky NI, Landrum JT, Bone RA (2003) Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr 23:171–201
Lepage C, Roy C (1984) Improved recovery of fatty acids through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396
Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
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
McGraw KJ, Ardia DR (2004) Immunoregulatory activity of different dietary carotenoids in male zebra finches. Chemoecology 14:25–29
Mínguez-Mosquera MI, Gandul-Rojas B, Gallardo-Guerrero ML (1992) Rapid method of quantification of chlorophylls and carotenoids in virgin olive oil by high-performance liquid chromatography. J Agric Food Chem 40:60–63
Moreno J, Rodríguez H, Vargas MA, Rivas J, Guerrero MG (1995) Nitrogen-fixing cyanobacteria as source of phycobiliprotein pigments. Composition and growth performance of ten filamentous heterocystous strains. J Appl Phycol 7:17–23
Niyogi KN, Björman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci U S A 94:14162–14167
Olaizola M (2000) Commercial production of astaxanthin from Haematococcus pluvialis using 25000-liter outdoor photobioreactors. J Appl Phycol 12:499–506
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
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
Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648
Richmond A (1986) Outdoor mass cultures of microalgae. In: Richmond A (ed) Handbooks of microalgal mass cultures. CRC Press, Boca Ratón, FL, pp 285–329
Rito-Palomares M, Negrete A, Miranda L, Flores C, Galindo E, Serrano-Carreon L (2001a) The potential application of aqueous two-phase systems for in situ recovery of 6-pentyl-infinity-pyrone produced by Trichoderma harzianum. Enzyme Microb Technol 28:625–631
Rito-Palomares M, Nuñez L, Amador D (2001b) Practical application of aqueous two-phase systems for the development of a prototype process for c-phycocyanin recovery from Spirulina maxima. J Chem Technol Biotechnol 76:1273–1280
Rodríguez-Ruiz J, Belarbi EH, García Sánchez JL, López Alonso D (1998) Rapid simultaneous lipid extraction and transesterification for fatty acid analysis. Biotechnol Tech 12:689–691
Sansawa H, Endo H (2004) Production of intracellular phytochemicals in Chlorella under heterotrophic conditions. J Biosci Bioeng 98:437–444
Shi XM, Zhang XW, Chen F (2000) Heterotrophic production of biomass and lutein by Chlorella protothecoides on various nitrogen sources. Enzyme Microb Technol 27:312–318
Shi XM, Jiang Y, Chen F (2002) High-yield production of lutein by the green microalga Chlorella protothecoides in heterotrophic fed-batch culture. Biotechnol Prog 18:723–727
Tredici M (2004) Mass production of microalgae: photobioreactors. In: Richmond A (ed) Handbook of microalgal culture. Blackwell, Oxford, UK, pp 178–214
Acknowledgements
This work was supported by Plan Nacional, Ministerio de Educación y Ciencia (grant nos. PPQ2001-3832-C02-01 and BIO2004-05834-C02-02, cofinanced with FEDER funds from EU), IFAPA (CO3-125), and Plan Andaluz de Investigación (group no. CVI131), Spain.
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Blanco, A.M., Moreno, J., Del Campo, J.A. et al. Outdoor cultivation of lutein-rich cells of Muriellopsis sp. in open ponds. Appl Microbiol Biotechnol 73, 1259–1266 (2007). https://doi.org/10.1007/s00253-006-0598-9
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DOI: https://doi.org/10.1007/s00253-006-0598-9