Physiology and adaptive significance of secondary carotenogenesis in green microalgae

Russian Journal of Plant Physiology

Volumn 60, Issue 1, 2013, Pages 1-13

  Solovchenko, A E ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b TIMIRYAZEV INSTITUTE OF PLANT PHYSIOLOGY   (Russian Federation)

Author keywords

carotene; astaxanthin; Dunaliella bardawil; green algae; Haematococcus pluvialis; oleosomes; photoadaptation; photodamage

Indexed keywords

ALGAE; CHLOROPHYTA; DUNALIELLA BARDAWIL; HAEMATOCOCCUS PLUVIALIS;

EID: 84871679366     PISSN: 10214437     EISSN: None     Source Type: Journal    
DOI: 10.1134/S1021443713010081     Document Type: Review

References (78)

1. Wang, B., Zarka, A., Trebst, A., and Boussiba, S., Astaxanthin Accumulation in Haematococcus pluvialis (Chlorophyceae) as an Active Photoprotective Process under High Irradiance, J. Phycol., 2003, vol. 39, pp. 1116-1124.
2. Zhang, D. H. and Lee, Y. K., Two-Step Process for Ketocarotenoid Production by a Green Alga Chlorococcum sp. Strain Ma-1, Appl. Microbiol. Biotechnol., 2001, vol. 55, pp. 537-540.
3. Remias, D., Lütz-Meindl, U., and Lütz, C., Photosynthesis, Pigments and Ultrastructure of the Alpine Snow Alga Chlamydomonas nivalis, Eur. J. Phycol., 2005, vol. 40, pp. 259-268.
4. Remias, D., Karsten, U., Lütz, C., and Leya, T., Physiological and Morphological Processes in the Alpine Snow Alga Chloromonas nivalis (Chlorophyceae) during Cyst Formation, Protoplasma, 2010, vol. 243, pp. 73-86.
5. Ladygin, V. G. and Shirshikova, G., Carotenoid Functions in Eukaryote Chloroplasts - Recent Concepts, Zh. Obshch. Biol., 2006, vol. 67, pp. 163-190.
6. Ben-Amotz, A., Shaish, A., and Avron, M., Mode of Action of the Massively Accumulated β-Carotene of Dunaliella bardawil in Protecting the Alga against Damage by Excess Irradiation, Plant Physiol., 1989, vol. 86, pp. 1286-1291.
7. Hagen, C., Braune, W., and Björn, L., Functional Aspects of Secondary Carotenoids in Haematococcus lacustris (Volvocales): 3. Action as a Sunshade, J. Phycol., 1994, vol. 30, pp. 241-248.
8. Solovchenko, A. E. and Merzlyak, M. N., Screening of Visible and UV Radiation as a Photoprotective Mechanism in Plants, Russ. J. Plant Physiol., 2008, vol. 55, pp. 719-737.
9. Lemoine, Y. and Schoefs, B., Secondary Ketocarotenoid Astaxanthin Biosynthesis in Algae: A Multifunctional Response to Stress, Photosynth. Res., 2010, vol. 106, pp. 155-177.
10. Kobayashi, M. and Sakamoto, Y., Singlet Oxygen Quenching Ability of Astaxanthin Esters from the Green Alga Haematococcus pluvialis, Biotechnol. Lett., 1999, vol. 21, pp. 265-269.
11. Boussiba, S., Carotenogenesis in the Green Alga Haematococcus pluvialis: Cellular Physiology and Stress Response, Physiol. Plant., 2000, vol. 108, pp. 111-117.
12. Czygan, F., Blood-Rain and Blood-Snow: Nitrogen-Deficient Cells of Haematococcus pluvialis and Chlamydomonas nivalis, Arch. Microbiol., 1970, vol. 74, pp. 69-76.
13. Bidigare, R., Ondrusek, M., Kennicutt, M., Iturriaga, R., Harvey, H., Hoham, R., and Macko, S., Evidence a Photoprotective for Secondary Carotenoids of Snow Algae, J. Phycol., 1993, vol. 29, pp. 427-434.
14. Ben-Amotz, A. and Avron, M., On the Factors which Determine Massive β-Carotene Accumulation in the Halotolerant Alga Dunaliella bardawil, Plant Physiol., 1983, vol. 72, pp. 593-597.
15. Palozza, P., Prooxidant Actions of Carotenoids in Biologic Systems, Nutr. Rev., 1998, vol. 56, pp. 257-265.
16. Nishino, H., Murakoshi, M., Tokuda, H., and Satomi, Y., Cancer Prevention by Carotenoids, Arch. Biochem. Biophys., 2009, vol. 483, pp. 165-168.
17. Ye, Z.-W., Jiang, J.-G., and Wu, G.-H., Biosynthesis and Regulation of Carotenoids in Dunaliella: Progresses and Prospects, Biotechnol. Adv., 2009, vol. 26, pp. 352-360.
18. Borowitzka, M., Carotenoid Production Using Microorganisms, Single Cell Oils, Cohen, Z., Ratledge, C., Eds., Champaign, Illinois: AOCS Press, 2005, pp. 124-137.
19. Cunningham, F., Jr. and Gantt, E., Genes and Enzymes of Carotenoid Biosynthesis in Plants, Annu. Rev. Plant Biol., 1998, vol. 49, pp. 557-583.
20. Ladygin, V. G., Biosynthesis of Carotenoids in Plant Plastids, Biokhimiya, 2000, vol. 65, pp. 1317-1333.
21. Boussiba, S. and Vonshak, A., Astaxanthin Accumulation in the Green Alga Haematococcus pluvialis, Plant Cell Physiol., 1991, vol. 32, pp. 1077-1082.
22. Britton, G., UV/Visible Spectroscopy, Carotenoids, Britton, G., Liaaen-Jensen, S., and Pfander, H., Eds., Basel: Birkhauser Verlag, 1995, pp. 13-62.
23. Green, B. and Durnford, D., The Chlorophyll-Carotenoid Proteins of Oxygenic Photosynthesis, Annu. Rev. Plant Biol., 1996, vol. 47, pp. 685-714.
24. Del Campo, J. A., Rodríguez, H., Moreno, J., Vargas, M., Rivas, J., and Guerrero, M. G., Lutein Production by Muriellopsis sp. in an Outdoor Tubular Photobioreactor, J. Biotechnol., 2001, vol. 85, pp. 289-295.
25. Del Campo, J., García-González, M., and Guerrero, M., Outdoor Cultivation of Microalgae for Carotenoid Production: Current State and Perspectives, Appl. Microbiol. Biotechnol., 2007, vol. 74, pp. 1163-1174.
26. Ben-Amotz, A., Katz, A., and Avron, M., Accumulation of β-Carotene in Halotolerant Alga: Purification and Characterization of β-Carotene-Rich Globules from Dunaliella bardawil (Chlorophyceae), J. Phycol., 1982, vol. 18, pp. 529-537.
27. Bar, E., Rise, M., Vishkautsan, M., and Arad, S., Pigment and Structural Changes in Chlorella zofingiensis upon Light and Nitrogen Stress, J. Plant Physiol., 1995, vol. 146, pp. 527-534.
28. Malis, S. A., Cohen, E., and Ben Amotz, A., Accumulation of Canthaxanthin in Chlorella emersonii, Physiol. Plant., 1993, vol. 87, pp. 232-236.
29. Pennington, F. C., Haxo, F. T., Borch, G., and Liaaen-Jensen, S., Carotenoids of Cryptophyceae, Biochem. Syst. Ecol., 1985, vol. 13, pp. 215-219.
30. Rabbani, S., Beyer, P., Lintig, J., Hugueney, P., and Kleinig, H., Induced β-Carotene Synthesis Driven by Triacylglycerol Deposition in the Unicellular Alga Dunaliella bardawil, Plant Physiol., 1998, vol. 116, pp. 1239-1248.
31. Grünewald, K., Eckert, M., Hirschberg, J., and Hagen, C., Phytoene Desaturase Is Localized Exclusively in the Chloroplast and Up-Regulated at the mRNA Level during Accumulation of Secondary Carotenoids in Haematococcus pluvialis (Volvocales, Chlorophyceae), Plant Physiol., 2000, vol. 122, pp. 1261-1268.
32. Lotan, T. and Hirschberg, J., Cloning and Expression in Escherichia coli of the Gene Encoding β-C-4-Oxygenase, That Converts β-Carotene to the Ketocarotenoid Canthaxanthin in Haematococcus pluvialis, FEBS Lett., 1995, vol. 364, pp. 125-128.
33. Fraser, P. D., Miura, Y., and Misawa, N., In Vitro Characterization of Astaxanthin Biosynthetic Enzymes, J. Biol. Chem., 1997, vol. 272, pp. 6128-6135.
34. Grünewald, K., Hirschberg, J., and Hagen, C., Ketocarotenoid Biosynthesis Outside of Plastids in the Unicellular Green Alga Haematococcus pluvialis, J. Biol. Chem., 2001, vol. 276, pp. 6023-6029.
35. Santos, M. F. and Mesquita, J., Ultrastructural Study of Haematococcus lacustris (Girod.) Rostafinski (Volvocales): 1. Some Aspects of Carotenogenesis, Cytology, 1984, vol. 49, pp. 215-228.
36. Vorst, P., Baard, R. L., Mur, L. R., Korthals, H. J., and Ende, H., Effect of Growth Arrest on Carotene Accumulation and Photosynthesis in Dunaliella, Microbiology, 1994, vol. 140, pp. 1411-1417.
37. Collins, A. M., Jones, H. D. T., Han, D., Hu, Q., Beechem, T. E., and Timlin, J. A., Carotenoid Distribution in Living Cells of Haematococcus pluvialis (Chlorophyceae), PLoS ONE, 2011, vol. 6, p. e24302.
38. Grünewald, K. and Hagen, C., β-Carotene Is the Intermediate Exported from the Chloroplast during Accumulation of Secondary Carotenoids in Haematococcus pluvialis, J. Appl. Phycol., 2001, vol. 13, pp. 89-93.
39. Jin, E., Polle, J., Lee, H., Hyun, S., and Chang, M., Xanthophylls in Microalgae: From Biosynthesis To Biotechnological Mass Production and Application, J. Microbiol. Biotechnol, 2003, vol. 13, pp. 165-174.
40. Solovchenko, A. E., Khozin-Goldberg, I., Didi-Cohen, S., Cohen, Z., and Merzlyak, M. N., Effects of Light and Nitrogen Starvation on the Content and Composition of Carotenoids of the Green Microalga Parietochloris incisa, Russ. J. Plant Physiol., 2008, vol. 55, pp. 455-462.
41. Kobayashi, M., Kakizono, T., and Nagai, S., Enhanced Carotenoid Biosynthesis by Oxidative Stress in Acetate-Induced Cyst Cells of a Green Unicellular Alga, Haematococcus pluvialis, Appl. Environ. Microbiol., 1993, vol. 59, pp. 867-873.
42. Fan, L., Vonshak, A., Zarka, A., and Boussiba, S., Does Astaxanthin Protect Haematococcus against Light Damage? Z. Naturforsch., C: BioSci., 1998, vol. 53, p. 93.
43. Pick, U., Dunaliella: A Model Extremophilic Alga, Isr. J. Plant Sci., 1998, vol. 46, pp. 131-139.
44. Steinbrenner, J. and Linden, H., Light Induction of Carotenoid Biosynthesis Genes in the Green Alga Haematococcus pluvialis: Regulation by Photosynthetic Redox Control, Plant Mol. Biol., 2003, vol. 52, pp. 343-356.
45. Jaspers, P. and Kangasjärvi, J., Reactive Oxygen Species in Abiotic Stress Signaling, Physiol. Plant., 2010, vol. 138, pp. 405-413.
46. Ip, P. and Chen, F., Employment of Reactive Oxygen Species to Enhance Astaxanthin Formation in Chlorella zofingiensis in Heterotrophic Culture, Pichia stipitis, Proc. Biochem., 2005, vol. 40, pp. 3491-3496.
47. Shaish, A., Avron, M., Pick, U., and Ben-Amotz, A., Are Active Oxygen Species Involved in Induction of β-Carotene in Dunaliella bardawil, Planta, 1993, vol. 190, pp. 363-368.
48. Semenenko, V. E. and Abdullaev, A. A., Parametric Control of β-Carotene Biosynthesis in Dunaliella bardawil Cells from Intense Culture Conditions, Sov. Plant Physiol., 1980, vol. 27, pp. 31-41.
49. Katz, A., Jimenez, C., and Pick, U., Isolation and Characterization of a Protein Associated with Carotene Globules in the Alga Dunaliella bardawil, Plant Physiol., 1995, vol. 108, pp. 1657-1664.
50. Abdullaev, A. A. and Semenenko, V. E., Some Physiological Characteristics of Dunaliella salina Teod. Intense Culture, Sov. Plant Physiol., 1974, vol. 21, pp. 1145-1153.
51. Droop, M., Carotenogenesis in Haematococcus pluvialis, Nature, 1955, vol. 175, p. 42.
52. Jahnke, L., Massive Carotenoid Accumulation in Dunaliella bardawil Induced by Ultraviolet-A Radiation, J. Photochem. Photobiol., B: Biol., 1999, vol. 48, pp. 68-74.
53. White, A. and Jahnke, L., Contrasting Effects of UV-A and UV-B on Photosynthesis and Photoprotection of β-Carotene in Two Dunaliella spp., Plant Cell Physiol., 2002, vol. 43, pp. 877-884.
54. Solovchenko, A., Khozin-Goldberg, I., Cohen, Z., and Merzlyak, M., Carotenoid-to-Chlorophyll Ratio as a Proxy for Assay of Total Fatty Acids and Arachidonic Acid Content in the Green Microalga Parietochloris incisa, J. Appl. Phycol., 2009, vol. 21, pp. 361-366.
55. Aflalo, C., Bing, W., Zarka, A., and Boussiba, S., The Effect of the Herbicide Glufosinate (Basta) on Astaxanthin Accumulation in the Green Alga Haematococcus pluvialis, Z. Naturforsch., C: BioSci., 1999, vol. 54, pp. 49-54.
56. Borowitzka, M. A., Borowitzka, L. J., and Kessly, D., Effects of Salinity Increase on Carotenoid Accumulation in the Green Alga Dunaliella salina, J. Appl. Phycol., 1990, vol. 2, pp. 111-119.
57. Mendoza, H., del Rio, M. J., Reina, G. G., and Ramazanov, Z., Low-Temperature-Induced Oil-Carotene and Fatty Acid Synthesis, and Ultrastructural Reorganization of the Chloroplast in Dunaliella salina (Chlorophyta), Eur. J. Phycol., 1996, vol. 31, pp. 329-331.
58. Abe, K., Mihara, H., and Hirano, M., Characteristics of Growth and Carotenoid Accumulation of the Aerial Microalga Trentepohlia aurea in Liquid Culture, J. Marin. Biotechnol., 1998, vol. 6, pp. 53-58.
59. Shi, X. M. and Chen, F., High-Yield Production of Lutein by the Green Microalga Chlorella protothecoides in Heterotrophic Fed-Batch Culture, Biotechnol. Prog., 2002, vol. 18, pp. 723-727.
60. Vladimirova, M. G., Ultrastructure of Dunaliella salina Cell and Its Functional Changes Depending on Light Intensity and Temperature, Sov. Plant Physiol., 1978, vol. 25, pp. 571-576.
61. Merzlyak, M., Chivkunova, O., Gorelova, O., Reshetnikova, I., Solovchenko, A., Khozin-Goldberg, I., and Cohen, Z., Effect of Nitrogen Starvation on Optical Properties, Pigments, and Arachidonic Acid Content of the Unicellular Green Alga Parietochloris incisa (Trebouxiophyceae, Chlorophyta), J. Phycol., 2007, vol. 43, pp. 833-843.
62. Peled, E., Leu, S., Zarka, A., Weiss, M., Pick, U., Khozin-Goldberg, I., and Boussiba, S., Isolation of a Novel Oil Globule Protein from the Green Alga Haematococcus pluvialis (Chlorophyceae), Lipids, 2011, vol. 46, pp. 851-861.
63. Zhekisheva, M., Boussiba, S., Khozin-Goldberg, I., Zarka, A., and Cohen, Z., Accumulation of Oleic Acid in Haematococcus pluvialis (Chlorophyceae) under Nitrogen Starvation or High Light Is Correlated with That of Astaxanthin Esters, J. Phycol., 2002, vol. 38, pp. 325-331.
64. Künzler, K. and Eichenberger, W., Betaine Lipids and Zwitterionic Phospholipids in Plants and Fungi, Phytochemisry, 1997, vol. 46, pp. 883-892.
65. Solovchenko, A., Merzlyak, M., Khozin-Goldberg, I., Cohen, Z., and Boussiba, S., Coordinated Carotenoid and Lipid Syntheses Induced in Parietochloris incisa (Chlorophyta, Trebouxiophyceae) Mutant Deficient in δ5 Desaturase by Nitrogen Starvation and High Light, J. Phycol., 2010, vol. 46, pp. 763-772.
66. Mendoza, H., Martel, A., del Rio, M. J., and Garcia, Reina, G., Oleic Acid Is the Main Fatty Acid Related with Carotenogenesis in Dunaliella salina, J. Appl. Phycol., 1999, vol. 11, pp. 15-19.
67. Zhekisheva, M., Zarka, A., Khozin-Goldberg, I., Cohen, Z., and Boussiba, S., Inhibition of Astaxanthin Synthesis under High Irradiance Does Not Abolish Triacylglycerol Accumulation in the Green Alga Haematococcus pluvialis (Chlorophyceae), J. Phycol., 2005, vol. 41, pp. 819-826.
68. Solovchenko, A. E., Physiological Role of Neutral Lipid Accumulation in Eukaryotic Microalgae under Stresses, Russ. J. Plant Physiol., 2012, vol. 59, pp. 167-176.
69. Hagen, C., Braune, W., and Greulich, F., Functional Aspects of Secondary Carotenoids in Haematococcus lacustris [Girod] Rostafinski (Volvocales). IV. Protection from Photodynamic Damage, J. Photochem. Photobiol., B: Biol., 1993, vol. 20, pp. 153-160.
70. Semenenko, V. E., Mechanisms of Photosynthesis Endogenous Regulation and Chloroplast Adaptive Features, Physiology of Photosynthesis, Nichiporovich, A. A., Ed., Moscow: Nauka, 1982, pp. 164-187.
71. Ramazanov, Z. M., Klyachko-Gurvich, G. L., Ksenofontov, A. L., and Semenenko, V. E., Effects of Suboptimal Temperature on β-Carotene and Lipids Contents in the Halophilic Alga Dunaliella salina, Sov. Plant Physiol., 1988, vol. 35, pp. 864-872.
72. Sun, Z., Cunningham, F. X., and Gantt, E., Differential Expression of Two Isopentenyl Pyrophosphate Isomerases and Enhanced Carotenoid Accumulation in a Unicellular Chlorophyte, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 11 482-11 488.
73. Solovchenko, A. E., Chivkunova, O. B., and Maslova, I. P., Pigment Composition, Optical Properties, and Resistance to Photodamage of the Microalga Haematococcus pluvialis Cultivated under High Light, Russ. J. Plant Physiol., 2011, vol. 58, pp. 9-17.
74. Kobayashi, M., In Vivo Antioxidant Role of Astaxanthin under Oxidative Stress in the Green Alga Haematococcus pluvialis, Appl. Microbiol. Biotechnol., 2000, vol. 54, pp. 550-555.
75. Li, Y., Sommerfeld, M., Chen, F., and Hu, Q., Consumption of Oxygen by Astaxanthin Biosynthesis: A Protective Mechanism against Oxidative Stress in Haematococcus pluvialis (Chlorophyceae), J. Plant Physiol., 2008, vol. 165, pp. 1783-1797.
76. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., and Darzins, A., Microalgal Triacylglycerols as Feedstocks for Biofuel Production: Perspectives and Advances, Plant J., 2008, vol. 54, pp. 621-639.
77. Merzlyak, M. N., Chivkunova, O. B., Maslova, I. P., Naqvi, R. K., Solovchenko, A. E., and Klyachko-Gurvich, G. L., Light Absorption and Scattering by Cell Suspensions of Some Cyanobacteria and Microalgae, Russ. J. Plant Physiol., 2008, vol. 55, pp. 420-425.
78. Solovchenko, A., Khozin, I., and Chivkunova, O., Real-Time Spectral Techniques for Detection of the Build up of Valuable Compounds and Stress in Microalgal Cultures: Implications for Biotechnology, Microalgae: Biotechnology, Microbiology and Energy, Johansen, M., Ed., Hauppauge, New York: Nova Sci. Publ., 2011, pp. 251-276.