Skip to main content

Advertisement

SpringerLink
Log in

Production of carotenoids by microalgae: achievements and challenges

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

An Erratum to this article was published on 04 August 2015

Abstract

Carotenoids are a wide group of lipophylic isoprenoids synthesized by all photosynthetic organisms and also by some non-photosynthetic bacteria and fungi. Animals, which cannot synthesize carotenoids de novo, must include them in their diet to fulfil essential provitamin, antioxidant, or colouring requirements. Carotenoids are indispensable in light harvesting and energy transfer during photosynthesis and in the protection of the photosynthetic apparatus against photooxidative damage. In this review, we outline the factors inducing carotenoid accumulation in microalgae, the knowledge acquired on the metabolic pathways responsible for their biosynthesis, and the recent achievements in the genetic engineering of this pathway. Despite the considerable progress achieved in understanding and engineering algal carotenogenesis, many aspects remain to be elucidated. The increasing number of sequenced microalgal genomes and the data generated by high-throughput technologies will enable a better understanding of carotenoid biosynthesis in microalgae. Moreover, the growing number of industrial microalgal species genetically modified will allow the production of novel strains with enhanced carotenoid contents.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Albrecht M, Misawa N, Sandmann G (1999) Metabolic engineering of the terpenoid biosynthetic pathway of Escherichia coli for production of the carotenoids β-carotene and zeaxanthin. Biotechnol Lett 21:791–795

    CAS  Google Scholar 

  • Álvarez R, Vaz B, Gronemeyer H, de Lera AR (2014) Functions, therapeutic applications, and synthesis of retinoids and carotenoids. Chem Rev 114:1–125

    PubMed  Google Scholar 

  • Ambati RR, Phang SM, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities, and its commercial applications—a review. Mar Drugs 12:128–152

    PubMed Central  PubMed  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    CAS  Google Scholar 

  • Bar E, Rise M, Vishkautsan M, Arad S (1995) Pigment and structural changes in Chlorella zofingiensis upon light and nitrogen stress. J Plant Physiol 146:527–534

    CAS  Google Scholar 

  • Baroli I, Do A, Yamane T, Niyogi KK (2003) Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15:992–1008

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ben-Amotz A, Katz A, Avron M (1982) Accumulation of β-carotene in halotolerant algae: purification and characterization of β-carotene-rich globules from Dunaliella bardawil (Chlorophyceae]. J Phycol 18:529–537

    CAS  Google Scholar 

  • Ben-Amotz A, Gressel J, Avron M (1987) Massive accumulation of phytoene induced by norflurazon in Dunaliella bardawil (Chlorophyceae) prevents recovery from photoinhibition. J Phycol 23:176–181

    CAS  Google Scholar 

  • Ben-Amotz A, Lers A, Avron M (1988) Stereoisomers of beta-carotene and phytoene in the alga Dunaliella bardawil. Plant Physiol 86:1286–1291

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ben-Amotz A, Shaish A, Avron M (1989) Mode of action of the massively accumulated β-carotene of Dunaliella bardawil in protecting the alga against damage by excess radiation. Plant Physiol 91:1040–1043

    PubMed Central  CAS  PubMed  Google Scholar 

  • Berla BM, Saha R, Immethun CM, Maranas CD, Moon TS, Pakrasi HB (2013) Synthetic biology of cyanobacteria: unique challenges and opportunities. Front Microbiol 27:246

    Google Scholar 

  • Bertrand M (2010) Carotenoid biosynthesis in diatoms. Photosynth Res 106:89–102

    CAS  PubMed  Google Scholar 

  • Bidgare RR, Ondrusek ME, Kennicutt MC, Iturriaga R, Harvey HR, Hoham RW, Macko SA (1993) Evidence a photoprotective for secondary carotenoids of snow algae. J Phycol 29:427–434

    Google Scholar 

  • Blount JD, McGraw KJ (2008) Signal functions of carotenoid colouration. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 4., Natural functionsBirkhäuser, Basel, pp 213–236

    Google Scholar 

  • Bohne F, Linden H (2002) Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinhardtii. Biochim Biophys Acta 1579:26–34

    CAS  PubMed  Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae-their development and commercialisation. J Appl Phycol 25:743–756

    CAS  Google Scholar 

  • Borowitzka LJ, Borowitzka MA, Moulton TP (1984) The mass culture of Dunaliella salina for fine chemicals: from laboratory to pilot plant. Hydrobiologia 116(117):115–134

    Google Scholar 

  • Borowitzka MA, Huisman JM, Osborn A (1991) Culture of the astaxanthin-producing green alga Haematococcus pluvialis. 1. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304

    CAS  Google Scholar 

  • Botella-Pavía P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A, Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40:188–199

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Bouvier F, Rahier A, Camara B (2005) Biogenesis, molecular regulation and function of plant isoprenoids. Prog Lipid Res 44:357–429

    CAS  PubMed  Google Scholar 

  • Breitenbach J, Zhu C, Sandmann G (2001) Bleaching herbicide norflurazon inhibits phytoene desaturase by competition with the cofactors. J Agric Food Chem 49:5270–5272

    CAS  PubMed  Google Scholar 

  • Britton G (2008) Functions of intact carotenoids. In: Britton G, Liaaen-Jensen S, Pfander H (eds) carotenoids, vol 4., Natural functionsBirkhäuser, Basel, pp 189–212

    Google Scholar 

  • Britton G (2009) Vitamin A and vitamin A deficiency. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 5., Nutrition and healthBirkhäuser, Basel, pp 173–190

    Google Scholar 

  • Britton G, Liaaen-Jensen S, Pfander H (2004) Carotenoids Handbook (Eds.), XI, Birkhäuser, Basel

  • Büch K, Stransky H, Hager A (1995) FAD is a further essential cofactor of the NAD(P)H and O2-dependent zeaxanthin-epoxidase. FEBS Lett 376:45–48

  • Capa-Robles W, Paniagua MJ, Soto JO (2009) The biosynthesis and accumulation of beta-carotene in Dunaliella salina proceed via the glyceraldehyde 3-phosphate/pyruvate pathway. Nat Prod Res 23:1021–1028

    CAS  PubMed  Google Scholar 

  • Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Func Plant Biol 38:833–847

    CAS  Google Scholar 

  • Cerutti H, Ma X, Msanne J, Repas T (2011) RNA-mediated silencing in algae: biological roles and tools for analysis of gene function. Eukaryot Cell 10:1164–1172

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chang MCY, Keasling JD (2006) Production of isoprenoid pharmaceuticals by engineered microbes. Nat Chem Biol 2:674–681

    CAS  PubMed  Google Scholar 

  • Chekanov K, Lobakova E, Selyakh I, Semenova L, Sidorov R, Solovchenko A (2014) Accumulation of astaxanthin by a new Haematococcus pluvialis strain BM1 from the White Sea coastal rocks (Russia). Mar Drugs 12:4504–4520

    PubMed Central  PubMed  Google Scholar 

  • Chinembiri TN, du Plessis LH, Gerber M, Hamman JH, du Plessis J (2014) Review of natural compounds for potential skin cancer treatment. Molecules 19:11679–11721

    PubMed  Google Scholar 

  • Chisté RC, Freitas M, Mercadante AZ, Fernandes E (2014) Carotenoids are effective inhibitors of in vitro hemolysis of human erythrocytes, as determined by a practical and optimized cellular antioxidant assay. J Food Sci 79:1841–1847

    Google Scholar 

  • Christaki E, Bonos E, Giannenas I, Florou-Paneri P (2012) Functional properties of carotenoids originating from algae. J Sci Food Agric 93:5–11

    PubMed  Google Scholar 

  • Coesel SN, Baumgartner AC, Teles LM, Ramos AA, Henriques NM, Cancela L, Varela JC (2008a) Nutrient limitation is the main regulatory factor for carotenoid accumulation and for Psy and Pds steady state transcript levels in Dunaliella salina (Chlorophyta) exposed to high light and salt stress. Mar Biotechnol 10:602–611

    CAS  PubMed  Google Scholar 

  • Coesel SN, Obornik M, Varela J, Falciatore A, Bowler C (2008b) Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms. PLoS ONE 3:e2896

    PubMed Central  PubMed  Google Scholar 

  • Cordero BF, Obraztsova I, Martín L, Couso I, León R, Vargas MA, Rodríguez H (2010) Isolation and characterization of a lycopene β-cyclase gene from the astaxanthin-producing green alga Chlorella zofingiensis (Chlorophyta). J Phycol 46:1229–1238

    CAS  Google Scholar 

  • Cordero BF, Couso I, León R, Rodríguez H, Vargas MA (2011) Enhancement of carotenoids biosynthesis in Chlamydomonas reinhardtii by nuclear transformation using a phytoene synthase gene isolated from Chlorella zofingiensis. Appl Microbiol Biotechnol 91:341–351

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cordero BF, Couso I, León R, Rodriguez H, Vargas MA (2012) Isolation and characterization of a lycopene ε-cyclase gene of Chlorella (Chromochloris) zofingiensis. Regulation of the carotenogenic pathway by nitrogen and light. Mar Drugs 10:2069–2088

    PubMed Central  CAS  PubMed  Google Scholar 

  • Couso I, Vila M, Rodriguez H, Vargas MA, León R (2011) Overexpression of an exogenous phytoene synthase gene in the unicellular alga Chlamydomonas reinhardtii leads to an increase in the content of carotenoids. Biotechnol Prog 27:54–60

    CAS  PubMed  Google Scholar 

  • Couso I, Vila M, Vigara J, Vargas MA, Rodríguez H, León R (2012) Synthesis of carotenoids and regulation of the carotenoid biosynthesis pathway in response to high light stress in microalgae. Eur J Phycol 47:223–232

    CAS  Google Scholar 

  • Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Ann Rev Plant Physiol Plant Mol Biol 49:557–583

    CAS  Google Scholar 

  • Cunningham FX Jr, Gantt E (2007) A portfolio of plasmids for identification and analysis of carotenoid pathway enzymes: Adonis aestivalis as a case study. Photosynth Res 92:245–259

    CAS  PubMed  Google Scholar 

  • Cunningham FX Jr, Pogson B, Sun Z, McDonald KA, DellaPenna D, Gantt E (1996) Functional analysis of the β- and ε-lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613–1626

    PubMed Central  CAS  PubMed  Google Scholar 

  • Davidi L, Shimoni E, Khozin-Goldberg I, Zamir A, Pick U (2014) Origin of β-carotene-rich plastoglobuli in Dunaliella bardawil. Plant Physiol 164:2139–2156

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A, Czygan FC (1989) Zeaxanthin synthesis, energy dissipation, and photoprotection of photosystem II at chilling temperatures. Plant Physiol 90:894–898

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dieser M, Greenwood M, Foreman CM (2010) Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Artic Antarctic Alpine Res 42:396–405

    Google Scholar 

  • Diretto G, Al-Babili S, Tavazza R, Papacchioli V, Beyer P, Giuliano G (2007) Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoS ONE 2:e350

    PubMed Central  PubMed  Google Scholar 

  • Dugas MB, Yeager J, Richards-Zawaki CL (2013) Carotenoid supplementation enhances reproductive success in captive strawberry poison frogs (Oophaga pumilio). Zoo Biol 32:655–658

    CAS  PubMed  Google Scholar 

  • Erickson E, Wakao S, Niyogi KK (2015) Light stress and photoprotection in Chlamydomonas reinhardtii. Plant J. doi:10.1111/tpj.12825

    PubMed  Google Scholar 

  • Ernst OP, Lodowski DT, Elstner M, Hegemann P, Brown LS, Kandori H (2014) Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem Rev 114:126–163

    PubMed Central  CAS  PubMed  Google Scholar 

  • Farré G, Sanahuja G, Naqvi S, Bai C, Capell T, Zhu C, Christou P (2010) Travel advice on the road to carotenoids in plants. Plant Sci 179:28–48

    Google Scholar 

  • Farré G, Riera SM, Alves R, Vilaprinyo E, Sorribas A, Canela R, Naqvi S, Sandmann G, Capell T, Zhu C, Christou P (2013) Targeted transcriptomic and metabolic profiling reveals temporal bottlenecks in the maize carotenoid pathway that may be addressed by multigene engineering. Plant J 75:441–455

    PubMed  Google Scholar 

  • Feng S, Xue L, Liu H, Lu P (2009) Improvement of efficiency of genetic transformation for Dunaliella salina by glass beads method. Mol Bio Rep 36:1433–1439

    CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    CAS  PubMed  Google Scholar 

  • Fraser PD, Romer S, Shipton CA, Mills PB, Kiano JW, Misawa N, Drake RG, Schuch W, Bramley PM (2002) Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci USA 99:1092–1097

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fučikova K, Lewis LA (2012) Intersection of Chlorella, Muriella and Bracteacoccus: Resurrecting the genus Chromochloris KOL et CHODAT (Chlorophyceae, Chlorophyta). Fottea 12:83–93

    Google Scholar 

  • Fujimaki H, Shiozawa S, Inoue M (2003) Effect of salty crust on soil albedo. Agr Forest Meteorol 118:125–135

    Google Scholar 

  • Giuliano G (2014) Plant carotenoids: genomics meets multi-gene engineering. Curr Opin Plant Biol 19:111–117

    CAS  PubMed  Google Scholar 

  • Giuliano G, Tavazza R, Diretto G, Beyer P, Taylor MA (2008) Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol 26:139–145

    CAS  PubMed  Google Scholar 

  • González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22:2058–2084

    PubMed Central  PubMed  Google Scholar 

  • Goold H, Beisson F, Peltier G, Li-Beisson Y (2015) Microalgal lipid droplets: composition, diversity, biogenesis and functions. Plant Cell Rep 34:545–555

    CAS  PubMed  Google Scholar 

  • Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122

    CAS  PubMed  Google Scholar 

  • Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32

    CAS  PubMed  Google Scholar 

  • Gouveia L, Empis J (2003) Relative stabilities of microalgal carotenoids in microalgal extracts, biomass and fish feed: effect of storage conditions. Innov Food Sci Emerging Technol 4:227–233

    CAS  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 

  • Guo S, Zhao X, Tang Y, Wan C, Alam MA, Ho S, Bai F, Chang J (2013) Establishment of an efficient genetic transformation system in Scenedesmus obliquus. J Biotechnol 163:61–68

    CAS  PubMed  Google Scholar 

  • Hager A (1970) Ausbildung von Maxima im Absorptionsspektrum von Carotinoiden im Bereich um 370 nm; Folgen für die Interpretation bestimmter Wirkungsspektren. Planta 91:38–53

    CAS  PubMed  Google Scholar 

  • Hakala M, Tuominen I, Keränen M, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochim Biophys Acta 1706:68–80

    CAS  PubMed  Google Scholar 

  • Harker M, Tsavalos AJ, Young AJ (1996) Factors responsible for astaxanthin formation in the chlorophyte Haematococcus pluvialis. Biores Technol 55:207–214

    CAS  Google Scholar 

  • Hieber AD, Bugos RC, Yamamoto HY (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta 1482:84–91

    CAS  PubMed  Google Scholar 

  • Huang JC, Wang Y, Sandmann G, Chen F (2006) Isolation and characterization of a carotenoid oxygenase gene from Chlorella zofingiensis (Chlorophyta). Appl Microbiol Biotechnol 71:473–479

    CAS  PubMed  Google Scholar 

  • Jahns P, Holzarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193

    CAS  PubMed  Google Scholar 

  • Jinkerson RE, Radakovits R, Posewitz MC (2013) Genomic insights from the oleaginous model alga Nannochloropsis gaditana. Bioengineered 4:37–43

    PubMed Central  PubMed  Google Scholar 

  • Kajiwara S, Kakizono T, Saito T, Kondo K, Ohtani T, Nishio N, Nagai S, Misawa N (1995) Isolation and functional identification of a novel cDNA for astaxanthin biosynthesis from Haematococcus pluvialis and astaxanthin synthesis in Escherichia coli. Plant Mol Biol 29:343–352

    CAS  PubMed  Google Scholar 

  • Kathiresan S, Chandrashekar A, Ravishankar GA, Sarada R (2009) Agrobacterium-mediated transformation in the green alga Haematococcus pluvialis (Chlorophyceae, Volvocales). J Phycol 45:642–649

    CAS  Google Scholar 

  • Kianianmomeni A (2014) Cell-type specific light-mediated transcript regulation in the multicellular alga Volvox carteri. BMC Genom 15:764

    Google Scholar 

  • Kilian O, Benemann CSE, Niyogi KK, Vick B (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc Natl Acad Sci USA 108:21265–21269

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kim J, DellaPenna D (2006) Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid beta-ring hydroxylase CYP97A3. Proc Natl Acad Sci USA 103:3474–3479

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kimura N, Shimada N (1988) Membrane-associated nucleoside diphosphate kinase from rat liver. Purification, characterization, and comparison with cytosolic enzyme. J Biol Chem 263:4647–4653

    CAS  PubMed  Google Scholar 

  • Kirk JT (1988) Solar heating of water bodies as influenced by their inherent optical properties. J Geophys Res 93:10897–10908

    Google Scholar 

  • Kobayashi M, Kakizono T, Yamaguchi K, Nishio N, Nagai S (1992) Growth and astaxanthin formation of Haematococcus pluvialis in heterotrophic and mixotrophic conditions. J Ferment Bioeng 74:17–20

    CAS  Google Scholar 

  • Kohn S, Kolbe H, Korger M, Köpsel C, Mayer B, Auweter H, Lüddecke E, Bettermann H, Martin H-D (2008) Aggregation and interface behaviour of carotenoids. In: Britton G, Liaaen-Jensen S, Pfander H (eds) carotenoids, vol 4., Natural functionsBirkhäuser, Basel, pp 53–98

    Google Scholar 

  • Kreimer G (2009) The green algal eyespot apparatus: a primordial visual system and more? Curr Genet 55:19–43

    CAS  PubMed  Google Scholar 

  • León R, Fernández E (2007) Nuclear transformation of eukaryotic microalgae: historical overview, achievements and problems. Adv Exp Med Biol 616:1–11

    PubMed  Google Scholar 

  • León R, Vila M, Hernánz D, Vílchez C (2005) Production of phytoene by herbicide-treated microalgae Dunaliella bardawil in two-phase systems. Biotechnol Bioeng 92:685–694

    Google Scholar 

  • León R, Couso I, Fernández E (2007) Metabolic engineering of ketocarotenoids biosynthesis in the unicellular microalga Chlamydomonas reinhardtii. J Biotechnol 130:143–152

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    CAS  PubMed  Google Scholar 

  • Liu J, Gerken H, Huang J, Chen F (2013) Engineering of an endogenous phytoene desaturase gene as a dominant selectable marker for Chlamydomonas reinhardtii transformation and enhanced biosynthesis of carotenoids. Process Biochem 48:788–795

    CAS  Google Scholar 

  • 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. Mar Drugs 12:3487–3515

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lohr M (2009) Carotenoids. In: Stern D (ed) The chlamydomonas sourcebook, vol 2., Organellar and Metabolic ProcessesElsevier, San Diego, pp 799–817

    Google Scholar 

  • Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci USA 96:8784–8789

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lohr M, Im CS, Grossman A (2005) Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 138:490–515

    PubMed Central  CAS  PubMed  Google Scholar 

  • Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157

    CAS  PubMed  Google Scholar 

  • Marri V, Richner H (2014) Yolk carotenoids increase fledging success in great tit nestlings. Oecologia 176:371–377

    PubMed  Google Scholar 

  • Masamoto K, Misawa N, Kaneko T, Kikuno R, Toh H (1998) β-carotene hydroxylase gene from the cyanobacterium Synechocystis sp. PCC6803. Plant Cell Physiol 39:560–564

    CAS  PubMed  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant Functions. Science 318:245–250

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miller R, Wu G, Deshpande RR, Vieler A, Gärtner K, Li X, Moellering ER, Zäuner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MH, Hegg EL, Shachar-Hill Y, Shiu SH, Benning C (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154:1737–1752

    PubMed Central  CAS  PubMed  Google Scholar 

  • Misawa N, Shimada H (1998) Metabolic engineering for the production of carotenoids in non-carotenogenic bacteria and yeasts. J Biotechnol 59:169–181

    CAS  Google Scholar 

  • Molnar A, Bassett A, Thuenemann E, Schwach F, Karkare S, Ossowski S, Weigel D, Baulcombe D (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J 58:165–174

    CAS  PubMed  Google Scholar 

  • Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75:50–59

    CAS  PubMed  Google Scholar 

  • Müller P, Li XP, Niyogi K (2001) Non-photochemical quenching. A response to excess energy. Plant Physiol 125:1558–1566

    PubMed Central  PubMed  Google Scholar 

  • Oren A (2009) Saltern evaporation ponds as model systems for the study of primary production processes under hypersaline conditions. Aquat Microb Ecol 56:193–204

    Google Scholar 

  • Oroud IM (2001) A new formulation of evaporation-temperature dynamics of saline solutions. Water Resour Res 37:2513–2520

    Google Scholar 

  • Paine JA, Shipton CA, Chaggar S, Howell RM, Kennedy MJ, Vernon G, Susan Y, Wright SY, Hinchliffe E, Adams JL, Aron L, Silverstone AL, Drake R (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23:482–487

    CAS  PubMed  Google Scholar 

  • Paiva SAR, Russell RM (1999) β-carotene and other carotenoids as antioxidants. J Am College Nutr 18:426–433

    CAS  Google Scholar 

  • Paniagua-Michel J, Olmos-Soto J, Ruiz MA (2012) Pathways of carotenoid biosynthesis in bacteria and microalgae. Methods Mol Biol 892:1–12

    CAS  PubMed  Google Scholar 

  • Pineau B, Gérard-Hirne C, Selve C (2001) Carotenoid binding to photosystems I and II of Chlamydomonas reinhardtii cells grown under weak light or exposed to intense light. Plant Physiol Biochem 39:73–85

    CAS  Google Scholar 

  • Pirastru L, Darwish M, Chu FL, Perreault F, Sirois L, Sleno L, Radovan Popovic R (2011) Carotenoid production and change of photosynthetic functions in Scenedesmus sp. exposed to nitrogen limitation and acetate treatment. J Appl Phycol 24:117–124

    Google Scholar 

  • Polívka T, Frank HA (2010) Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc Chem Res 43:1125–1134

    PubMed Central  PubMed  Google Scholar 

  • Purton S (2007) Tools and techniques for chloroplast transformation of Chlamydomonas. Adv Exp Med Biol 616:34–45

    PubMed  Google Scholar 

  • Quesada-Vargas T, Ruiz ON, Daniell H (2005) Characterization of heterologous multigene operons in transgenic chloroplasts. Transcription, processing, and translation. Plant Physiol 138:1746–1762

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rabbani S, Beyer P, Hugueney LP, Kleinig H (1998) Induced β-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116:1239–1248

    PubMed Central  CAS  PubMed  Google Scholar 

  • Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3:686

    PubMed Central  PubMed  Google Scholar 

  • Ramos A, Coesel S, Marques A, Rodrigues M, Baumgartner A, Noronha J, Rauter A, Brenig B, Varela J (2008) Isolation and characterization of a stress-inducible Dunaliella salina Lcy-β gene encoding a functional lycopene beta-cyclase. Appl Microbiol Biotechnol 79:819–828

    CAS  PubMed  Google Scholar 

  • Ramos AA, Polle JJ, Tran D, Cushman JC, Jin E, Varela JC (2011) The unicellular green alga Dunaliella salina Teod. as a model for abiotic stress tolerance: genetic advances and future perspectives. Algae 26:3–20

    CAS  Google Scholar 

  • Ruff MD, Fuller HL (1975) Carotenoid levels in chickens infected with EImeria acervulina or E. tenella. J Nutr 105:1447–1456

    CAS  PubMed  Google Scholar 

  • Salguero A, León R, Mariotti A, de la Morena B, Vega JM, Vílchez C (2005) UV-A mediated induction of carotenoid accumulation in Dunaliella bardawil with retention of cell viability. Appl Microbiol Biotechnol 66:506–511

    CAS  PubMed  Google Scholar 

  • Sandmann G (2001) Genetic manipulation of carotenoid biosynthesis: strategies, problems and achievements. Trends Plant Sci 6:114–117

    Google Scholar 

  • Sandmann G, Römer S, Fraser PD (2006) Understanding carotenoid metabolism as a necessity for genetic engineering of crop plants. Metab Eng 8:291–302

    CAS  PubMed  Google Scholar 

  • Sasso S, Pohnert G, Lohr M, Mittag M, Hertweck C (2012) Microalgae in the postgenomic era: a blooming reservoir for new natural products. FEMS Microbiol Rev 36:761–785

    CAS  PubMed  Google Scholar 

  • Schmidt-Dannert C, Umeno D, Arnol FH (2000) Molecular breeding of carotenoid biosynthetic pathways. Nat Biotechnol 18:750–753

    CAS  PubMed  Google Scholar 

  • Schwender J, Gemünden C, Lichtenthaler HK (2001) Chlorophyta exclusively use the 1-deoxyxylulose 5-phosphate/2-C-methylerythritol 4-phosphate pathway for the biosynthesis of isoprenoids. Planta 212:416–423

    CAS  PubMed  Google Scholar 

  • Sistrom WR, Clayton RK (1964) Studies on a mutant of Rhodopseudomonas spheroides unable to grow photosynthetically. Biochim Biophys Acta 88:61–73

    CAS  PubMed  Google Scholar 

  • Smith BM, Morrissey PJ, Guenther JE, Nemson JA, Harrison MA, Allen JF, Melis A (1990) Response of the photosynthetic apparatus in Dunaliella salina (green algae) to irradiance stress. Plant Physiol 93:1433–1440

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stahl W, Sies H (2007) Carotenoids and flavonoids contribute to nutritional protection against skin damage from sunlight. Mol Biotechnol 37:26–30

    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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stoddard MC (2012) Mimicry and masquerade from the avian visual perspective. Curr Zool 58:630–648

    Google Scholar 

  • Sun F, Huo X, Zhai Y, Wang A, Xu J, Su D, Bartlam M, Rao Z (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121:1043–1057

    CAS  PubMed  Google Scholar 

  • Sun G, Zhang X, Sui Z, Mao Y (2008) Inhibition of pds gene expression via the RNA interference approach in Dunaliella salina (Chlorophyta). Mar Biotechnol 10:219–226

    CAS  PubMed  Google Scholar 

  • Sun TH, Liu CQ, Hui YY, Wu WK, Zhou ZG, Lu S (2010) Coordinated regulation of gene expression for carotenoid metabolism in Chlamydomonas reinhardtii. J Integr Plant Biol 52:868–878

    CAS  PubMed  Google Scholar 

  • Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9:1101–1118

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tan C, Quinn S, Zhang Q, Jiang P, Zhao F (2005) Establishment of a micro-particle bombardment transformation system for Dunaliella salina. J Microbiol 43:361–365

    CAS  PubMed  Google Scholar 

  • Tang G, Russell RM (2009) Carotenoids as provitamin A. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 5., Nutrition and healthBirkhäuser, Basel, pp 149–172

    Google Scholar 

  • Telfer A, Pascal A, Gall A (2008) Carotenoids in photosynthesis. In: Britton G, Liaaen-Jensen S, Pfander J (eds) Carotenoids, vol 4., Natural functionsBirkhäuser, Basel, pp 265–308

    Google Scholar 

  • Teng C, Qin S, Liu J, Yu D, Liang C, Tseng C (2002) Transient expression of lacZ in bombarded unicellular green alga Haematococcus pluvialis. J Appl Phycol 14:497–500

    CAS  Google Scholar 

  • Tian L, Magallanes-Lundback M, Musetti V, DellaPenna D (2003) Functional analysis of beta- and epsilon-ring carotenoid hydroxylases in Arabidopsis. Plant Cell 15:1320–1332

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tsuchihashi H, Kigoshi M, Iwatsuki M, Niki E (1995) Action of β-carotene as an antioxidant against lipid peroxidation. Arch Biochem Biophys 323:137–147

    CAS  PubMed  Google Scholar 

  • Úbeda-Mínguez P, Chileh T, Dautor Y, García-Maroto F, Alonso D (2014) Tools for microalgal biotechnology: development of an optimized transformation method for an industrially promising microalga—Tetraselmis chuii. J Appl Phycol 27:223–232

    Google Scholar 

  • Vidhyavathi R, Venkatachalam L, Sarada R, Ravishankar GA (2008) Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions. J Exp Bot 59:1409–1418

    CAS  PubMed  Google Scholar 

  • Vila M, Couso I, León R (2008) Carotenoid content in mutants of the chlorophyte Chlamydomonas reinhardtii with low expression levels of phytoene desaturase. Process Biochem 43:1147–1152

    CAS  Google Scholar 

  • Vílchez C, Forján E, Cuaresma M, Bédmar F, Garbayo I, Vega JM (2011) Marine carotenoids: biological functions and commercial applications. Mar Drugs 9:319–333

    PubMed Central  PubMed  Google Scholar 

  • Wang B, Zarka A, Trebst A, Boussiba S (2005) Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance. J Phycol 39:1116–1124

    Google Scholar 

  • Ye ZW, Jiang JG, Wu GH (2008) Biosynthesis and regulation of carotenoids in Dunaliella: progresses and prospects. Biotechnol Adv 26:352–360

    CAS  PubMed  Google Scholar 

  • Yin Q, Ma Y, Hong Y, Hou X, Chen J, Shen C, Sun M, Shang Y, Dong S, Zeng Z, Pei J-J, Liu X (2014) Lycopene attenuates insulin signaling deficits, oxidative stress, neuroinflammation, and cognitive impairment in fructose-drinking insulin resistant rats. Neuropharmacol 86:389–396

    CAS  Google Scholar 

  • Zhang H, Huang D, Cramer WA (1999) Stoichiometrically bound β-carotene in the cytochrome b 6 f complex of oxygenic photosynthesis protects against oxygen damage. J Biol Chem 274:1581–1587

    CAS  PubMed  Google Scholar 

  • Zhang X-S, Zhang X, Wu Q, Li W, Wang C-X, Xie G-B, Zhou X-M, Shi J-X, Zhou M-L (2014) Astaxanthin offers neuroprotection and reduces neuroinflammation in experimental subarachnoid haemorrhage. J Surgical Res 192:206–213

    CAS  Google Scholar 

  • Zorin B, Lu Y, Sizova I, Hegemann P (2009) Nuclear gene targeting in Chlamydomonas as exemplified by disruption of the PHOT gene. Gene 432:91–96

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Andalusian government (Project P09-CVI-5053 and BIO214) and the Foundation for Science and Technology (FCT), Portugal, via the XTREMEBIO project (PTDC/MAR-EST/4346/2012). This is a publication (No. 94) from CEIMAR Publication Series.

Author information

Authors and Affiliations

  1. Centre of Marine Science, University of Algarve, Campus de Gambelas, Faro, Portugal

    João C. Varela & Hugo Pereira

  2. Laboratory of Biochemistry and Molecular Biology, University of Huelva, Marine International Campus of Excellence (CEIMAR), Huelva, Spain

    Hugo Pereira, Marta Vila & Rosa León

Authors
  1. João C. Varela
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hugo Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marta Vila
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rosa León
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosa León.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Varela, J.C., Pereira, H., Vila, M. et al. Production of carotenoids by microalgae: achievements and challenges. Photosynth Res 125, 423–436 (2015). https://doi.org/10.1007/s11120-015-0149-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0149-2

Keywords

Search

Navigation