Skip to main content
Log in

Outdoor cultivation of lutein-rich cells of Muriellopsis sp. in open ponds

  • Biotechnological Products and Process Engineering
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  • Apt K, Behrens P (1999) Commercial developments in microalgal biotechnology. J Phycol 35:215–226

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for marineculture. Aquaculture 151:315–331

    Article  CAS  Google Scholar 

  • Chew BP (1996) Importance of antioxidant vitamins in immunity and health in animals. Anim Feed Sci Technol 59:103–114

    Article  CAS  Google Scholar 

  • 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

    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

    Article  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

    Article  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(6):848–854

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Goldman JC (1979) Outdoor algal mass cultures. II. Photosynthetic field limitations. Water Res 13:119–160

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Jiménez C, Cossío BR, Labella D, Niell FX (2003) The feasibility of industrial production of Spirulina (Arthrospira) in southern Spain. Aquaculture 217:179–190

    Article  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

    Article  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

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lepage C, Roy C (1984) Improved recovery of fatty acids through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  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 

  • McGraw KJ, Ardia DR (2004) Immunoregulatory activity of different dietary carotenoids in male zebra finches. Chemoecology 14:25–29

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Niyogi KN, Björman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci U S A 94:14162–14167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olaizola M (2000) Commercial production of astaxanthin from Haematococcus pluvialis using 25000-liter outdoor photobioreactors. J Appl Phycol 12:499–506

    Article  CAS  Google Scholar 

  • 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

    Article  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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miguel G. Guerrero.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-006-0598-9

Keywords

Navigation