Abstract
Various carotenoids of the cyanobacterium Prochlorococcus sp. are identified using chromatographic/spectroscopic techniques and quantified using HPLC-DAD. In the present study, β-apo-8′-carotenal was used as internal standard. Identification of carotenoids was carried out by comparing the retention time, absorption spectra, and mass spectra of unknown peaks with reference standards. All-trans-lutein was found to be the major carotenoid in this cyanobacterium, and, therefore, algal productivity and the potential for lutein accumulation were analyzed as a function of different nitrogen sources such as nitrate, nitrite, ammonia, and urea for cultivation. Among them, urea clearly led to the best lutein accumulation. According to the experimental evidence, lutein increased from 2.54 to 3.34 mg g−1 in the cyanobacteria when urea was used as the nitrogen source.
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Amorim-Carrilho K, Cepeda A, Fente C, Regal P (2014) Review of methods for analysis of carotenoids. Trends Anal Chem 56:49–73
Andersen RA, Berges JA, Harrisson PJ, Watanabe MM (2005) Recipes for freshwater and seawater media. In: Anderson RA (ed) Algal culturing techniques. Elsevier Academic Press, Amsterdam, pp 429–538
Arnal E, Miranda M, Almansa I, Muriach M, Barcia JM, Romero FJ, Diaz-Llopis M, Bosch-Morell F (2009) Lutein prevents cataract development and progression in diabetic rats. Graefes Arch Clin Exp Ophthalmol 247:115–120
Astorg P (1997) Food carotenoids and cancer prevention: an overview of current research. Trends Food Sci Technol 8:406–413
Becker EW (1993) Microalgae: biotechnology and microbiology,. Cambridge University Press
Becker W (2004) Microalgae in human and animal nutrition. In: Richmond A (ed) Microalgal culture: biotechnology and applied phycology. Blackwell Science, Oxford, pp 312–351
Bendich A, Olson JA (1989) Biological actions of carotenoids. FASEB J 3:1927–1932
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
Borowitzka MA (2010) Carotenoid production using microorganisms. In: Cohen Z, Ratledge C (eds) Single cell oils. Microbial and algal oils. AOCS Press, Urbana, pp 225–240
Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756
Borowitzka MA, Borowitzka LJ (1988) Limits to growth and carotenogenesis in laboratory and large-scale outdoor cultures of Dunaliella salina. In: Stadler T, Mollion J, Verdus MC, Karamanos Y, Morvan H, Christiaen D (eds) Algal biotechnology. Elsevier Applied Science, Barking, pp 371–381
Britton G, Liaaen-Jensen S, Pfander H, Mercadante AZ, Egeland ES (2004) Carotenoids – Handbook. Birkhäuser Verlag, Basel, CH
Del Campo JA, Rodriguez H, Moreno J, Vargas M, Rivas J, Guerrero MG (2001) Lutein production by Muriellopsis sp. in an outdoor tubular photobioreactor. J Biotechnol 85:289–295
Delcourt C, Carriere I, Delage M, Barberger-Gateau P, Schalch W (2006) Plasma lutein and zeaxanthin and other carotenoids as modifiable risk factors for age-related maculopathy and cataract: the POLA Study. Invest Ophthalmol Vis Sci 47:2329–2335
Demmig-Adams B, Adams WW (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153
Dwyer JH, Navab M, Dwyer KM, Hassan K, Sun P, Shircore A, Hama-Levy S, Hough G, Wang X, Drake T (2001) Oxygenated carotenoid lutein and progression of early atherosclerosis the Los Angeles atherosclerosis study. Circulation 103:2922–2927
Erdoğan A, Çağır A, Dalay MC, Eroğlu AE (2015) Composition of carotenoids in Scenedesmus protuberans: application of chromatographic and spectroscopic methods. Food Anal Methods 8:1970–1978
Fernández-Sevilla J, Acién Fernández F, Molina Grima E (2010) Biotechnological production of lutein and its applications. Appl Microbiol Biotechnol 86:27–40
Goldman JC (1977) Biomass production in mass cultures of marine phytoplankton at varying temperatures. J Exp Mar Biol Ecol 27:161–169
Granado F, Olmedilla B, Blanco I (2003) Nutritional and clinical relevance of lutein in human health. Br J Nutr 90:487–502
Heber D, Lu QY (2002) Overview of mechanisms of action of lycopene. Exp Biol Med 227:920–923
Hsieh C-H, Wu W-T (2009) Cultivation of microalgae for oil production with a cultivation strategy of urea limitation. Bioresour Technol 100:3921–3926
Jin E, Polle JE, Lee H, Hyun S, Chang M (2003) Xanthophylls in microalgae: from biosynthesis to biotechnological mass production and application. J Microbiol Biotechnol 13:165–174
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
Le Marchand L, Hankin JH, Kolonel LN, Beecher GR, Wilkens LR, Zhao LP (1993) Intake of specific carotenoids and lung cancer risk. Cancer Epidemiol Biomarkers Prev 2:183–187
Li Y, Horsman M, Wang B, Wu N, Lan CQ (2008) Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Appl Microbiol Biotechnol 81:629–636
Lin J-H, Lee D-J, Chang J-S (2015) Lutein production from biomass: marigold flowers versus microalgae. Bioresour Technol 184:421–428
Manke Natchigal A, Oliveira Stringheta A, Corrêa Bertoldi M, Stringheta P (2010) Quantification and characterization of lutein from Tagetes (Tagetes patula L.) and Calendula (Calendula officinalis L.) flowers. In: XXVIII International Horticultural Congress on Science and Horticulture for People (IHC2010): International Symposium on 939, 2010. pp 309–314
Moeller SM, Jacques PF, Blumberg JB (2000) The potential role of dietary xanthophylls in cataract and age-related macular degeneration. J Am Coll Nutr 19(supl 5):522S–527S
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. J Sci Food Agric 81:904–909
Perez-Garcia O, Escalante FM, de-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36
Rangel-Yagui CO, Danesi EDG, de Carvalho JCM, Sato S (2004) Chlorophyll production from Spirulina platensis: cultivation with urea addition by fed-batch process. Bioresour Technol 92:133–141
Richmond A (1990) Large scale microalgal culture and applications. Prog Clin Biol Res 7:269–330
Sánchez J, Fernández J, Acién F, Rueda A, Pérez-Parra J, Molina E (2008) Influence of culture conditions on the productivity and lutein content of the new strain Scenedesmus almeriensis. Process Biochem 43:398–405
Sánchez-Luna LD, Converti A, Tonini GC, Sato S, de Carvalho J (2004) Continuous and pulse feedings of urea as a nitrogen source in fed-batch cultivation of Spirulina platensis. Aquac Eng 31:237–245
Shi XM, Chen F, Yuan JP, Chen H (1997) Heterotrophic production of lutein by selected Chlorella strains. J Appl Phycol 9:445–450
Shi XM, Liu HJ, Zhang XW, Chen F (1999) Production of biomass and lutein by Chlorella protothecoides at various glucose concentrations in heterotrophic cultures. Process Biochem 34:341–347
Shi X-M, Zhang X-W, Chen F (2000) Heterotrophic production of biomass and lutein by Chlorella protothecoides on various nitrogen sources. Enzyme Microb Technol 27:312–318
Soletto D, Binaghi L, Lodi A, Carvalho J, Converti A (2005) Batch and fed-batch cultivations of Spirulina platensis using ammonium sulphate and urea as nitrogen sources. Aquaculture 243:217–224
Stengel E, Soeder C (1975) Control of photosynthetic production in aquatic ecosystems. In: Cooper JP (ed) Photosynthesis and productivity in different environments. Cambridge University Press, Cambridge, pp 645–660
Wei D, Chen F, Chen G, Zhang X, Liu L, Zhang H (2008) Enhanced production of lutein in heterotrophic Chlorella protothecoides by oxidative stress. Scı Chına Ser C 51(12):1088–1093
Zhang J, Sun Z, Sun P, Chen T, Chen F (2014) Microalgal carotenoids: beneficial effects and potential in human health. Food Funct 5:413–425
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The authors would like to acknowledge the Scientific and Technological Research Council of Turkey for the support of this work through the project TBAG 110T099 and also the Center of Material’s Research at İzmir Institute of Technology for the facilities (SEM and Elemental Analyzer).
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Erdoğan, A., Demirel, Z., Eroğlu, A.E. et al. Carotenoid Profile in Prochlorococcus sp. and Enrichment of Lutein Using Different Nitrogen Sources. J Appl Phycol 28, 3251–3257 (2016). https://doi.org/10.1007/s10811-016-0861-0
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DOI: https://doi.org/10.1007/s10811-016-0861-0