Journal of Plant Molecular Breeding

Micro Algal pigments: An introduction to their biosynthesis, applications and genetic engineering

Document Type : Review paper

Authors

1 Department of Plant Biotechnology, College of Agriculture, Jahrom University, Jahrom, Iran

2 Plant Genetic and Production, Faculty of Agriculture, Urmia University

3 Industrial Microbial Biotechnology Department, Research Institute for Industrial Biotechnology (RIIB), Academic Center for Education, Culture and Research (ACECR), Khorasan Razavi, Mashhad, Iran

Abstract

Algae are an enormous biological group, forming 50% of photosynthetic organisms. In addition to having chlorophyll for the absorption of light photons, algae are rich in red, orange, and yellow carotenoids, which mainly protect cells against harmful radiation and free radicals. Moreover, these organisms have phycobiliproteins (red and blue pigments), which are involved in capturing and passing light energy to chlorophylls during photosynthesis and have a wide range of antioxidant properties. Algae also play a key role in substituting artificial colorants with natural colorants due to the adverse side-effects of chemical colorants, especially since natural colors are commonly used by individuals and various industries. Recently, algal pigments have been widely used in medical, nutraceutical, cosmeceutical, and pharmaceutical industries owing to their antioxidant, antidiabetic, anti-obesity, anti-inflammatory, antiaging, antimalarial, and neuroprotective properties. The growing demand for algal bioproducts highlights the importance of evaluating the trends influential factors in their production. The current review study provided an introduction to algal pigment classification, distribution, function, application, and biological production. In addition, we have discussed crucial biochemical pathways, enzymes, and gene/biotechnological modifications, such as transformation and expression regulation, which noticeably affect the metabolism of their sink and source.

Keywords

[1]    John, D.M. 1994 Biodiversity and conservation: an algal perspective. Phycol. 38 3–15.
[2]    Keykha, F., Ameri, M., and Fakhrfeshani, M. 2020 The growth and pigment production rate of Spirulina platensis, under different light conditions. in: 7th Natl. Congr. Biol. Nat. Sci. Iran, Tehranpp. 5–9.
[3]    Gantt, E. and Cunningham, F.X. 2001 Algal pigments. Encyclopedia of life sciences.
[4]    Mulders, K.J.M., Lamers, P.P., Martens, D.E., and Wijffels, R.H. 2014 Phototrophic pigment production with microalgae: Biological constraints and opportunities. J. Phycol. 50 (2), 229–242.
[5]    Lamers, P.P., Janssen, M., De Vos, R.C.H., Bino, R.J., and Wijffels, R.H. 2008 Exploring and exploiting carotenoid accumulation in Dunaliella salina for cell-factory applications. Trends Biotechnol. 26 (11), 631–638.
[6]    Wright, S.W. and Jeffrey, S.W. 2006 Pigment markers for phytoplankton production. Handb. Environ. Chem. Vol. 2 React. Process. 2 N 71–104.
[7]    Chakdar, H. and Pabbi, S. 2017 Algal Pigments for Human Health and Cosmeceuticals. in: Algal Green Chem. Recent Prog. Biotechnol., Elsevier, pp. 171–188.
[8]    Ameri, M., Gord-Noshahri, N., Ghazi-Birgandi, R., and Ghassam, B.J. 2019 Evaluation of different extraction methods for phycocyanin extraction from Spirulina platensis. J. Phycol. Res. 1–7.
[9]    Begum, H., Yusoff, F.M.D., Banerjee, S., Khatoon, H., and Shariff, M. 2016 Availability and Utilization of Pigments from Microalgae. Crit. Rev. Food Sci. Nutr. 56 (13), 2209–2222.
[10]  Prasanna, R., Sood, A., Suresh, A., Nayak, S., and Kaushik, B.D. 2007 Potentials and applications of algal pigments in biology and industry. Acta Bot. Hung. 49 (1–2), 131–156.
[11]  Dufossé, L., Galaup, P., Yaron, A., Arad, S.M., Blanc, P., Murthy, K.N.C., et al. 2005 Microorganisms and microalgae as sources of pigments for food use: A scientific oddity or an industrial reality? in: Trends Food Sci. Technol., Elsevier, pp. 389–406.
[12]  Pareek, S., Sagar, N.A., Sharma, S., Kumar, V., Agarwal, T., González-Aguilar, G.A., et al. 2017 Chlorophylls: Chemistry and Biological Functions. in: Fruit Veg. Phytochem., John Wiley & Sons, Ltd, Chichester, UKpp. 269–284.
[13]  Nakamura, A., Akai, M., Yoshida, E., Taki, T., and Watanabe, T. 2003 Reversed-phase HPLC determination of chlorophyll a’ and phylloquinone in Photosystem I of oxygenic photosynthetic organisms. Universal existence of one chlorophyll a’ molecule in Photosystem I. Eur. J. Biochem. 270 (11), 2446–2458.
[14]  Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W., and Krauß, N. 2001 Three-dimensional structure of cyanobaoterial photosystem I at 2.5 Å resolution. Nature. 411 (6840), 909–917.
[15]  Humphrey, A.M. 2006 Chlorophyll as a Color and Functional Ingredient. J. Food Sci. 69 (5), C422–C425.
[16]  Scheer, H. n.d. STRUCTURE AND OCCURRENCE OF CHLOROPHYLLS I . INTRODUCTION. Chem. Chlorophylls. 3–30.
[17]  Niedzwiedzki, D.M. and Blankenship, R.E. 2010 Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls. Photosynth. Res. 106 (3), 227–238.
[18]  Cubas, C., Gloria Lobo, M., and González, M. 2008 Optimization of the extraction of chlorophylls in green beans (Phaseolus vulgaris L.) by N,N-dimethylformamide using response surface methodology. J. Food Compos. Anal. 21 (2), 125–133.
[19]  Stein, H. 1969 Salt Toleration by Plants : Enhancement with Calcium Rat Heart Papillary Muscles : Action Potentials and Mechanical Response to Paired Stimuli. 175 (1963), 49–50.
[20]  Holt, A.S. 1961 FURTHER EVIDENCE OF THE RELATION BETWEEN 2-DESVINYL-2-FORMYL-CHLOROPHYLL- a AND CHLOROPHYLL- d. Can. J. Bot. 39 (2), 327–331.
[21]  Holt, A.S. and Morley, H. V. 1959 A PROPOSED STRUCTURE FOR CHLOROPHYLL d. Can. J. Chem. 37 (3), 507–514.
[22]  Larkum, A.W.D. and Kühl, M. 2005 Chlorophyll d: The puzzle resolved. Trends Plant Sci. 10 (8), 355–357.
[23]  Chen, M., Schliep, M., Willows, R.D., Cai, Z.L., Neilan, B.A., and Scheer, H. 2010 A red-shifted chlorophyll. Science (80-. ). 329 (5997), 1318–1319.
[24]  Willows, R.D., Li, Y., Scheer, H., and Chen, M. 2013 Structure of chlorophyll f. Org. Lett. 15 (7), 1588–1590.
[25]  Tanaka, R. and Tanaka, A. 2007 Tetrapyrrole Biosynthesis in Higher Plants. Annu. Rev. Plant Biol. 58 (1), 321–346.
[26]  Hori, N. and Kumar, A.M. 1996 5-aminolevulinic acid formation in Arabidopsis thaliana. Plant Physiol. Biochem. 34 (1), 3–9.
[27]  Louie, G. V., Brownlie, P.D., Lambert, R., Cooper, J.B., Blundell, T.L., Wood, S.P., et al. 1992 Structure of porphobilinogen deaminase reveals a flexible multidomain polymerase with a single catalytic site. Nature. 359 (6390), 33–39.
[28]  Henríquez, V., Escobar, C., Galarza, J., and Gimpel, J. 2016 Carotenoids in microalgae. Subcell. Biochem. 79 219–237.
[29]  Vershinin, A. 1999 Biological functions of carotenoids - Diversity and evolution. in: BioFactors, IOS Press, pp. 99–104.
[30]  Kovary, K., Louvain, T.S., e Silva, M.C.C., Albano, F., Pires, B.B.M., Laranja, G.A.T., et al. n.d. Biochemical behaviour of norbixin during in vitro DNA damage induced by reactive oxygen species. Br. J. Nutr. 85 (04), 431.
[31]  Gong, Y. and Miao, X. 2019 Short chain fatty acid biosynthesis in microalgae synechococcus sp. PCC 7942. Mar. Drugs. 17 (5), 255.
[32]  Britton, G., Liaaen-Jensen, S., and Pfander, H. 2008 Special Molecules, Special Properties. in: Carotenoids, Birkhäuser Basel, pp. 1–6.
[33]  Polle, J.E.W., Calhoun, S., McKie-Krisberg, Z., Prochnik, S., Neofotis, P., Yim, W.C., et al. 2020 Genomic adaptations of the green alga Dunaliella salina to life under high salinity. Algal Res. 50 (June), 101990.
[34]  Lichtenthaler, H.K., Rohmer, M., and Schwender, J. 1997 Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol. Plant. 101 (3), 643–652.
[35]  Rohmer, M. 2007 Diversity in isoprene unit biosynthesis: The methylerythritol phosphate pathway in bacteria and plastids. Pure Appl. Chem. 79 (4), 739–751.
[36]  Ladygin, V.G. 2000 Biosynthesis of carotenoids in the chloroplasts of algae and higher plants. Russ. J. Plant Physiol. 47 (6), 796–814.
[37]  Soltani, N., Saberi Najafi, M., and Ameri, M. 2016 The effect of immobilization of Scenedesmus sp. ISC 109 on potential of reduction of Chromium. J. Aquat. Ecol. 5 (3), 80–88.
[38]  Sánchez, J.F., Fernández-Sevilla, J.M., Acién, F.G., Cerón, M.C., Pérez-Parra, J., and Molina-Grima, E. 2008 Biomass and lutein productivity of Scenedesmus almeriensis: Influence of irradiance, dilution rate and temperature. Appl. Microbiol. Biotechnol. 79 (5), 719–729.
[39]  Sandmann, G. 2009 Evolution of carotene desaturation: The complication of a simple pathway. Arch. Biochem. Biophys. 483 (2), 169–174.
[40]  Ye, Z.W., Jiang, J.G., and Wu, G.H. 2008 Biosynthesis and regulation of carotenoids in Dunaliella: Progresses and prospects. Biotechnol. Adv. 26 (4), 352–360.
[41]  Pandey, V.D., Pandey, A., and Sharma, V. 2013 Biotechnological applications of cyanobacterial phycobiliproteins. Int. J. Curr. Microbiol. App. Sci. 2 89–97.
[42]  NIU, J.F., WANG, G.C., Lin, X. zhi, and Zhou, B.C. 2007 Large-scale recovery of C-phycocyanin from Spirulina platensis using expanded bed adsorption chromatography. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 850 (1–2), 267–276.
[43]  Han, C., Takayama, S., and Park, J. 2015 Formation and manipulation of cell spheroids using a density adjusted PEG/DEX aqueous two phase system. Sci. Rep. 5.
[44]  Meurs, K.M., Lacombe, V.A., Dryburgh, K., Fox, P.R., Reiser, P.R., and Kittleson, M.D. 2006 Differential expression of the cardiac ryanodine receptor in normal and arrhythmogenic right ventricular cardiomyopathy canine hearts. 111–118.
[45]  Romay, C., Gonzalez, R., Ledon, N., Remirez, D., and Rimbau, V. 2005 C-Phycocyanin: A Biliprotein with Antioxidant, Anti-Inflammatory and Neuroprotective Effects. Curr. Protein Pept. Sci. 4 (3), 207–216.
[46]  Manirafasha, E., Ndikubwimana, T., Zeng, X., Lu, Y., and Jing, K. 2016 Phycobiliprotein: Potential microalgae derived pharmaceutical and biological reagent. Biochem. Eng. J. 109 282–296.
[47]  Kathiresan, S., Sarada, R., Bhattacharya, S., and Ravishankar, G.A. 2007 Culture media optimization for growth and phycoerythrin production fromPorphyridium purpureum. Biotechnol. Bioeng. 96 (3), 456–463.
[48]  Stadnichuk, I.N., Krasilnikov, P.M., and Zlenko, D. V. 2015 Cyanobacterial phycobilisomes and phycobiliproteins. Microbiol. (Russian Fed. 84 (2), 101–111.
[49]  Biswas,  avijit 2011 Identification and characterization of enzymes involved in the biosynthesis of different phycobiliproteins in cyanobacteria. .
[50]  Cornejo, J. and Beale, S.I. 1997 Phycobilin biosynthetic reactions in extracts of cyanobacteria. Photosynth. Res. 51 (3), 223–230.
[51]  Ameri, M., Baron-Sola, A., Khavari-Nejad, R.A., Soltani, N., Najafi, F., Bagheri, A., et al. 2020 Aluminium triggers oxidative stress and antioxidant response in the microalgae Scenedesmus sp. J. Plant Physiol. 246–247 153114.
[52]  Hemlata and Fatma, T. 2009 Screening of cyanobacteria for phycobiliproteins and effect of different environmental stress on its yield. Bull. Environ. Contam. Toxicol. 83 (4), 509–515.
[53]  Kagawa, T. and Suetsugu, N. 2007 Photometrical analysis with photosensory domains of photoreceptors in green algae. FEBS Lett. 581 (3), 368–374.
[54]  Grossman, A.R., Schaefer, M.R., Chiang, G.G., and Collier, J.L. 1993 Environmental effects on the light-harvesting complex of cyanobacteria. J. Bacteriol. 175 (3), 575–582.
[55]  Pisal, D.S. and Lele, S.S. 2005 Carotenoid production from microalga, Dunaliella salina. .
[56]  Domínguez-Bocanegra, A.R., Guerrero Legarreta, I., Martinez Jeronimo, F., and Tomasini Campocosio, A. 2004 Influence of environmental and nutritional factors in the production of astaxanthin from Haematococcus pluvialis. Bioresour. Technol. 92 (2), 209–214.
[57]  Kebede, E. and Ahlgren, G. 1996 Optimum growth conditions and light utilization efficiency of Spirulina platensis (= Arthrospira fusiformis) (Cyanophyta) from Lake Chitu, Ethiopia. Hydrobiologia. 332 (2), 99–109.
[58]  Kim, Z.H., Kim, S.H., Lee, H.S., and Lee, C.G. 2006 Enhanced production of astaxanthin by flashing light using Haematococcus pluvialis. Enzyme Microb. Technol. 39 (3), 414–419.
[59]  Rodríguez, H., Rivas, J., Guerrero, M.G., and Losada, M. 1991 Enhancement of phycobiliprotein production in nitrogen-fixing cyanobacteria. J. Biotechnol. 20 (3), 263–270.
[60]  Carvalho, A.P. and Malcata, F.X. 2003 Kinetic Modeling of the Autotrophic Growth of Pavlova lutheri: Study of the Combined Influence of Light and Temperature. Biotechnol. Prog. 19 (4), 1128–1135.
[61]  García-González, M., Moreno, J., Manzano, J.C., Florencio, F.J., and Guerrero, M.G. 2005 Production of Dunaliella salina biomass rich in 9-cis-β-carotene and lutein in a closed tubular photobioreactor. J. Biotechnol. 115 (1), 81–90.
[62]  Alam, M.A., Xu, J.L., and Wang, Z. 2020 Microalgae biotechnology for food, health and high value products. Springer Singapore, .
[63]  Keykha, F., Ameri, M., and Fakhrfeshani, M. 2020 Effects of salinity stress carotenoid and phycocianin and biomass production of Spirulina platensis. in: 7th Natl. Congr. Biol. Nat. Sci. Iran, Tehranpp. 1–5.  
[64]  Griffiths, M., Harrison, S.T.L., Smit, M., and Maharajh, D. 2016 Major Commercial Products from Micro- and Macroalgae. in: F. Bux, Y. Chisti (Eds.), Algae Biotechnol. Prod. Process., Springer International Publishing, Champp. 269–300.
[65]  Tossavainen, M., Ilyass, U., Ollilainen, V., Valkonen, K., Ojala, A., and Romantschuk, M. 2019 Influence of long term nitrogen limitation on lipid, protein and pigment production of Euglena gracilis in photoheterotrophic cultures. PeerJ. 7 e6624.
[66]  Zhao, L.-S., Li, K., Wang, Q.-M., Song, X.-Y., Su, H.-N., Xie, B.-B., et al. 2017 Nitrogen Starvation Impacts the Photosynthetic Performance of Porphyridium cruentum as Revealed by Chlorophyll a Fluorescence. Sci. Rep. 7 (1), 8542.
[67]  Yaakob, M.A., Mohamed, R.M., Al-Gheethi, A., Aswathnarayana Gokare, R., and Ambati, R.R. 2021 Influence of Nitrogen and Phosphorus on Microalgal Growth, Biomass, Lipid, and Fatty Acid Production: An Overview. Cells . 10 (2),.
[68]  Keykha, F., Mortazavi, Z., Kazemi, M., Mizani, F., Kafie, H., Ameri, M., et al. 2019 Effect of Nitrogen Sources on Spirulina Growth. in: 2nd Iran. Confrence Phycol., Phycological Society of Iran, Tehran.
[69]  Keykha, F., Mizani, F., Mortazavi, Z., and Kazemi, M. 2019 Different Values of Fertilizer, Salt and NaNO3 on Spirulina biomass and pigments production. in: 2nd Iran. Conf. Phycol., Phycological Society of Iran, Tehran.
[70]  Gord-Noshahri, N., Ameri, M., and Ghasem, B.J. 2019 Spirulina Production in Different Sources of Nitrogen. J. Phycol. Res.
[71]  Sangeetha, R.K. and Baskaran, V. 2010 Carotenoid composition and retinol equivalent in plants of nutritional and medicinal importance: Efficacy of β-carotene from Chenopodium album in retinol-deficient rats. Food Chem. 119 (4), 1584–1590.
[72]  Manivasagan, P., Bharathiraja, S., Santha Moorthy, M., Mondal, S., Seo, H., Dae Lee, K., et al. 2018 Marine natural pigments as potential sources for therapeutic applications. Crit. Rev. Biotechnol. 38 (5), 745–761.
[73]  Halim, R., Hosikian, A., Lim, S., and Danquah, M.K. 2010 Chlorophyll extraction from microalgae: A review on the process engineering aspects. Int. J. Chem. Eng.
[74]  Lanfer-Marquez, U.M., Barros, R.M.C., and Sinnecker, P. 2005 Antioxidant activity of chlorophylls and their derivatives. in: Food Res. Int., Elsevier, pp. 885–891.
[75]  JAMA 1936 CHLOROPHYLL AND BLOOD REGENERATION. J. Am. Med. Assoc. 106 (11), 925.
[76]  Bowers, W.F. 1947 Chlorophyll in wound healing and suppurative disease. Am. J. Surg. 73 (1), 37–50.
[77]  Ferruzzi, M.G. and Blakeslee, J. 2007 Digestion, absorption, and cancer preventative activity of dietary chlorophyll derivatives. Nutr. Res. 27 (1), 1–12.
[78]  Chuyen, H. Van and Eun, J.B. 2017 Marine carotenoids: Bioactivities and potential benefits to human health. Crit. Rev. Food Sci. Nutr. 57 (12), 2600–2610.
[79]  Varela, J.C., Pereira, H., Vila, M., and León, R. 2015 Production of carotenoids by microalgae: Achievements and challenges. Photosynth. Res. 125 (3), 423–436.
[80]  Fiedor, J. and Burda, K. 2014 Potential role of carotenoids as antioxidants in human health and disease. Nutrients. 6 (2), 466–488.
[81]  Pashkow, F.J., Watumull, D.G., and Campbell, C.L. 2008 Astaxanthin: A Novel Potential Treatment for Oxidative Stress and Inflammation in Cardiovascular Disease. Am. J. Cardiol. 101 (10 SUPPL.), S58–S68.
[82]  Martínez Andrade, K., Lauritano, C., Romano, G., and Ianora, A. 2018 Marine Microalgae with Anti-Cancer Properties. Mar. Drugs. 16 (5), 165.
[83]  Hasani-Ranjbar, S., Jouyandeh, Z., and Abdollahi, M. 2013 A systematic review of anti-obesity medicinal plants - an update. J. Diabetes Metab. Disord. 12 (1),.
[84]  Hayato, M., Masashi, H., Tokutake, S., Katsura, M.-F., and Kazuo, M. 2009 Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol. Med. Rep. 02 (06), 897–902.
[85]  Kim, K.N., Heo, S.J., Yoon, W.J., Kang, S.M., Ahn, G., Yi, T.H., et al. 2010 Fucoxanthin inhibits the inflammatory response by suppressing the activation of NF-κB and MAPKs in lipopolysaccharide-induced RAW 264.7 macrophages. Eur. J. Pharmacol. 649 (1–3), 369–375.
[86]  Kaewkroek, K., Wattanapiromsakul, C., Matsuda, H., Nakamura, S., and Tewtrakul, S. 2017 Anti-inflammatory activity of compounds from Kaempferia marginata rhizomes. Songklanakarin J. Sci. Technol. 39 (1), 91–99.
[87]  Tanaka, T., Shnimizu, M., and Moriwaki, H. 2012 Cancer chemoprevention by carotenoids. Molecules. 17 (3), 3202–3242.
[88]  Gammone, M., Riccioni, G., and D’Orazio, N. 2015 Marine Carotenoids against Oxidative Stress: Effects on Human Health. Mar. Drugs. 13 (10), 6226–6246.
[89]  Ameri, M., Kazemi, M., Mizani, F., and Mortazavi, Z. 2019 Biomass and Phycocyanin Production in Spirulina under Various Salt Concentration. in: 2nd Iran. Conf. Phycol., Phycological Society of Iran, Tehran.
[90]  Fayyaz, M., Chew, K.W., Show, P.L., Ling, T.C., Ng, I.S., and Chang, J.S. 2020 Genetic engineering of microalgae for enhanced biorefinery capabilities. Biotechnol. Adv. 43 107554.
[91]  Saini, D.K., Chakdar, H., Pabbi, S., and Shukla, P. 2020 Enhancing production of microalgal biopigments through metabolic and genetic engineering. Crit. Rev. Food Sci. Nutr. 60 (3), 391–405.
[92]  Couso, I., Vila, M., Rodriguez, H., Vargas, M.A., and 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 (1), 54–60.
[93]  Vidhyavathi, R., Venkatachalam, L., Sarada, R., and Ravishankar, G.A. 2008 Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions. J. Exp. Bot. 59 (6), 1409–1418.
[94]  Liu, J., Sun, Z., Gerken, H., Liu, Z., Jiang, Y., and Chen, F. 2014 Chlorella zofingiensis as an alternative microalgal producer of astaxanthin: Biology and industrial potential. Mar. Drugs. 12 (6), 3487–3515.
[95]  Galarza, J.I., Gimpel, J.A., Rojas, V., Arredondo-Vega, B.O., and Henríquez, V. 2018 Over-accumulation of astaxanthin in Haematococcus pluvialis through chloroplast genetic engineering. Algal Res. 31 291–297.
[96]  Zhekisheva, M., Zarka, A., Khozin-Goldberg, I., Cohen, Z., and Boussiba, S. 2005 INHIBITION OF ASTAXANTHIN SYNTHESIS UNDER HIGH IRRADIANCE DOES NOT ABOLISH TRIACYLGLYCEROL ACCUMULATION IN THE GREEN ALGA HAEMATOCOCCUS PLUVIALIS (CHLOROPHYCEAE)1. J. Phycol. 41 (4), 819–826.
[97]  Lemoine, Y. and Schoefs, B. 2010 Secondary ketocarotenoid astaxanthin biosynthesis in algae: A multifunctional response to stress. Photosynth. Res. 106 (1–2), 155–177.
[98]  Naghshbandi, M.P., Tabatabaei, M., Aghbashlo, M., Gupta, V.K., Sulaiman, A., Karimi, K., et al. 2019 Progress toward improving ethanol production through decreased glycerol generation in Saccharomyces cerevisiae by metabolic and genetic engineering approaches. Renew. Sustain. Energy Rev. 115 109353.
[99]  Ameri, M., Khavari-Nejad, R.A., Soltani, N., Najafi, F., and Bagheri, A. 2020 Application of immobilized microalgae for native wastewater treatment. Algologia. 30 (1), 62–73.
[100]       Ng, W.S. n.d. Harvesting Micro Algae: The Green Gold of The Future.
[101]       Ng, I., Keskin, B.B., and Tan, S. 2020 A critical review of genome editing and synthetic biology applications in metabolic engineering of microalgae and cyanobacteria. Biotechnol. J. 15 (8), 1900228.
[102]       Nakamura, K. 2007 Chapter 3 - Future directions in photosynthetic organisms-catalyzed reactions. in: T.B.T.-F.D. in B. Matsuda (Ed.), Elsevier Science B.V., Amsterdampp. 51–58.
[103]       Benmoussa, M. 2016 Algomics for the Development of a Sustainable Microalgae Biorefinery. Single Cell Biol. 05 (01),.
[104]       n.d. National Alliance for Advanced Biofuels and Bioproducts Synopsis (NAABB) | Department of Energy.
[105]       Spicer, A. and Molnar, A. 2018 Gene Editing of Microalgae: Scientific Progress and Regulatory Challenges in Europe. Biology (Basel). 7 (1), 21.
[106]       Yahia, E.M. 2017 Fruit and Vegetable Phytochemicals. John Wiley & Sons, Ltd, Chichester, UK.
[107]       Din, A., Wani, M.A., Malik, S.A., Iqbal, S., Nazki, I.T., Naqash, F., et al. n.d. Biosynthesis and Degradation of Carotenoids in Ornamental Crops with specific reference to Chrysanthemum. Int. J. Environ. Agric. Biotechnol. 2 (2), 784–798.
[108]       Cordero, B.F., Couso, I., León, R., Rodríguez, H., and Vargas, M.Á. 2011 Enhancement of carotenoids biosynthesis in Chlamydomonas reinhardtii by nuclear transformation using a phytoene synthase gene isolated from Chlorella zofingiensis. Appl. Microbiol. Biotechnol. 91 (2), 341–351.
[109]       Perrine, Z., Negi, S., and Sayre, R.T. 2012 Optimization of photosynthetic light energy utilization by microalgae. Algal Res. 1 (2), 134–142.
[110]       Liu, J., Gerken, H., Huang, J., and 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 (5–6), 788–795.
[111]       Liu, J., Sun, Z., Gerken, H., Huang, J., Jiang, Y., and Chen, F. 2014 Genetic engineering of the green alga Chlorella zofingiensis: A modified norflurazon-resistant phytoene desaturase gene as a dominant selectable marker. Appl. Microbiol. Biotechnol. 98 (11), 5069–5079.
[112]       Eilers, U., Bikoulis, A., Breitenbach, J., Büchel, C., and Sandmann, G. 2016 Limitations in the biosynthesis of fucoxanthin as targets for genetic engineering in Phaeodactylum tricornutum. J. Appl. Phycol. 28 (1), 123–129.
[113]       Anila, N., Simon, D.P., Chandrashekar, A., Ravishankar, G.A., and Sarada, R. 2016 Metabolic engineering of Dunaliella salina for production of ketocarotenoids. Photosynth. Res. 127 (3), 321–333.
[114]       Chen, J.W., Liu, W.J., Hu, D.X., Wang, X., Balamurugan, S., Alimujiang, A., et al. 2017 Identification of a malonyl CoA-acyl carrier protein transacylase and its regulatory role in fatty acid biosynthesis in oleaginous microalga Nannochloropsis oceanica. Biotechnol. Appl. Biochem. 64 (5), 620–626.
[115]       Baek, K., Yu, J., Jeong, J., Sim, S.J., Bae, S., and Jin, E. 2018 Photoautotrophic production of macular pigment in a Chlamydomonas reinhardtii strain generated by using DNA-free CRISPR-Cas9 RNP-mediated mutagenesis. Biotechnol. Bioeng. 115 (3), 719–728.
[116]       Xue, J., Niu, Y.F., Huang, T., Yang, W.D., Liu, J.S., and Li, H.Y. 2015 Genetic improvement of the microalga Phaeodactylum tricornutum for boosting neutral lipid accumulation. Metab. Eng. 27 1–9.
[117]       Kang, N.K., Jeon, S., Kwon, S., Koh, H.G., Shin, S.E., Lee, B., et al. 2015 Effects of overexpression of a bHLH transcription factor on biomass and lipid production in Nannochloropsis salina. Biotechnol. Biofuels. 8 (1),.
[118]       Kaye, Y., Grundman, O., Leu, S., Zarka, A., Zorin, B., Didi-Cohen, S., et al. 2015 Metabolic engineering toward enhanced LC-PUFA biosynthesis in Nannochloropsis oceanica: Overexpression of endogenous δ12 desaturase driven by stress-inducible promoter leads to enhanced deposition of polyunsaturated fatty acids in TAG. Algal Res. 11 387–398.
[119]       Ngan, C.Y., Wong, C.-H., Choi, C., Yoshinaga, Y., Louie, K., Jia, J., et al. 2015 Lineage-specific chromatin signatures reveal a regulator of lipid metabolism in microalgae. Nat. Plants. 1 (8), 15107.
[120]       Li, D.W., Cen, S.Y., Liu, Y.H., Balamurugan, S., Zheng, X.Y., Alimujiang, A., et al. 2016 A type 2 diacylglycerol acyltransferase accelerates the triacylglycerol biosynthesis in heterokont oleaginous microalga Nannochloropsis oceanica. J. Biotechnol. 229 65–71.
[121]       Chen, C.-Y., Kao, A.-L., Tsai, Z.-C., Chow, T.-J., Chang, H.-Y., Zhao, X.-Q., et al. 2016 Expression of type 2 diacylglycerol acyltransferse gene DGTT1 from Chlamydomonas reinhardtii enhances lipid production in Scenedesmus obliquus. Biotechnol. J. 11 (3), 336–344.
[122]       Bajhaiya, A.K., Dean, A.P., Zeef, L.A.H., Webster, R.E., and Pittman, J.K. 2016 PSR1 is a global transcriptional regulator of phosphorus deficiency responses and carbon storage metabolism in Chlamydomonas reinhardtii. Plant Physiol. 170 (3), 1216–1234.
[123]       Shi, H., Chen, H., Gu, Z., Zhang, H., Chen, W., and Chen, Y.Q. 2016 Application of a delta-6 desaturase with α-linolenic acid preference on eicosapentaenoic acid production in Mortierella alpina. Microb. Cell Fact. 15 (1), 117.
[124]       Chen, C.Y., Kao, A.L., Tsai, Z.C., Shen, Y.M., Kao, P.H., Ng, I.S., et al. 2017 Expression of Synthetic Phytoene Synthase Gene to Enhance β-Carotene Production in Scenedesmus sp. CPC2. Biotechnol. J. 12 (11), 170–204.
[125]       Wei, H., Shi, Y., Ma, X., Pan, Y., Hu, H., Li, Y., et al. 2017 A type-I diacylglycerol acyltransferase modulates triacylglycerol biosynthesis and fatty acid composition in the oleaginous microalga, Nannochloropsis oceanica. Biotechnol. Biofuels. 10 (1), 174.
[126]       Kang, N.K., Kim, E.K., Kim, Y.U., Lee, B., Jeong, W.J., Jeong, B.R., et al. 2017 Increased lipid production by heterologous expression of AtWRI1 transcription factor in Nannochloropsis salina. Biotechnol. Biofuels. 10 (1),.
[127]       Zienkiewicz, K., Zienkiewicz, A., Poliner, E., Du, Z.Y., Vollheyde, K., Herrfurth, C., et al. 2017 Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts. Biotechnol. Biofuels. 10 (1), 8.
[128]       Tan, K.W.M. and Lee, Y.K. 2017 Expression of the heterologous Dunaliella tertiolecta fatty acyl-ACP thioesterase leads to increased lipid production in Chlamydomonas reinhardtii. J. Biotechnol. 247 60–67.
[129]       Matthijs, M., Fabris, M., Obata, T., Foubert, I., Franco‐Zorrilla, J.M., Solano, R., et al. 2017  The transcription factor bZIP14 regulates the TCA cycle in the diatom Phaeodactylum tricornutum . EMBO J. 36 (11), 1559–1576.
[130]       Li, Z., Meng, T., Ling, X., Li, J., Zheng, C., Shi, Y., et al. 2018 Overexpression of Malonyl-CoA: ACP Transacylase in Schizochytrium sp. to Improve Polyunsaturated Fatty Acid Production. J. Agric. Food Chem. 66 (21), 5382–5391.
[131]       Fan, Y., Yuan, C., Jin, Y., Hu, G.R., and Li, F.L. 2018 Characterization of 3-ketoacyl-coA synthase in a nervonic acid producing oleaginous microalgae Mychonastes afer. Algal Res. 31 225–231.
[132]       Wang, X., Dong, H.P., Wei, W., Balamurugan, S., Yang, W.D., Liu, J.S., et al. 2018 Dual expression of plastidial GPAT1 and LPAT1 regulates triacylglycerol production and the fatty acid profile in Phaeodactylum tricornutum 06 Biological Sciences 0601 Biochemistry and Cell Biology. Biotechnol. Biofuels. 11 (1), 1–14.
[133]       Kwon, S., Kang, N.K., Koh, H.G., Shin, S.E., Lee, B., Jeong, B.R., et al. 2018 Enhancement of biomass and lipid productivity by overexpression of a bZIP transcription factor in Nannochloropsis salina. Biotechnol. Bioeng. 115 (2), 331–340.
[134]       Salas-Montantes, C.J., González-Ortega, O., Ochoa-Alfaro, A.E., Camarena-Rangel, R., Paz-Maldonado, L.M.T., Rosales-Mendoza, S., et al. 2018 Lipid accumulation during nitrogen and sulfur starvation in Chlamydomonas reinhardtii overexpressing a transcription factor. J. Appl. Phycol. 30 (3), 1721–1733.
[135]       Poliner, E., Pulman, J.A., Zienkiewicz, K., Childs, K., Benning, C., and Farré, E.M. 2018 A toolkit for Nannochloropsis oceanica CCMP1779 enables gene stacking and genetic engineering of the eicosapentaenoic acid pathway for enhanced long-chain polyunsaturated fatty acid production. Plant Biotechnol. J. 16 (1), 298–309.
[136]       Osorio, H., Jara, C., Fuenzalida, K., Rey-Jurado, E., and Vásquez, M. 2019 High-efficiency nuclear transformation of the microalgae Nannochloropsis oceanica using Tn5 Transposome for the generation of altered lipid accumulation phenotypes. Biotechnol. Biofuels. 12 (1),.
[137]       Wang, F., Bi, Y., Diao, J., Lv, M., Cui, J., Chen, L., et al. 2019 Metabolic engineering to enhance biosynthesis of both docosahexaenoic acid and odd-chain fatty acids in Schizochytrium sp. S31. Biotechnol. Biofuels. 12 (1), 141.
[138]       Jia, B., Xie, X., Wu, M., Lin, Z., Yin, J., Lou, S., et al. 2019 Understanding the functions of endogenous DOF transcript factor in Chlamydomonas reinhardtii. Biotechnol. Biofuels. 12 (1),.
[139]       Li, D.W., Balamurugan, S., Yang, Y.F., Zheng, J.W., Huang, D., Zou, L.G., et al. 2019 Transcriptional regulation of microalgae for concurrent lipid overproduction and secretion. Sci. Adv. 5 (1),.
[140]       Shin, Y.S., Jeong, J., Nguyen, T.H.T., Kim, J.Y.H., Jin, E.S., and Sim, S.J. 2019 Targeted knockout of phospholipase A2 to increase lipid productivity in Chlamydomonas reinhardtii for biodiesel production. Bioresour. Technol. 271 368–374.
Journal of Plant Molecular Breeding
Volume 9, Issue 1
June 2021
Pages 42-61
  • Receive Date: 19 December 2020
  • Revise Date: 12 September 2021
  • Accept Date: 13 September 2021
  • First Publish Date: 13 September 2021