ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Stress-induced secondary carotenogenesis in Coelastrella rubescens (Scenedesmaceae, Chlorophyta), a producer of value-added keto-carotenoids

  • Received : 2017.02.01
  • Accepted : 2017.08.06
  • Published : 2017.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

We report on the culture growth and stress-induced secondary carotenogenesis in a biotechnologically promising but largely unexplored chlorophyte Coelastrella rubescens strain Vinatzer/Innsbruck V 195. Changes in the cell morphometry, biomass accumulation, its carotenoid and fatty acid profiles were followed in the cultures supplemented with either inorganic ($CO_2$) or organic (sodium acetate) carbon on the background of low-pH stress. Collectively, the results of the study characterize C. rubescens as a biotechnologically promising, potentially double-purpose organism. It produces several secondary keto-carotenoids with a considerable proportion of astaxanthin and canthaxanthin. At the same time, the cell lipid fatty acid profile of this microalga is suitable for obtaining a high-quality biodiesel complying with the strictest EN14214 European standard.

Keywords

References

  1. Abe, K., Hattori, H. & Hirano, M. 2007. Accumulation and antioxidant activity of secondary carotenoids in the aerial microalga Coelastrella striolata var. multistriata. Food Chem. 100:656-661. https://doi.org/10.1016/j.foodchem.2005.10.026
  2. Ahlgren, G. & Merino, L. 1991. Lipid analysis of freshwater microalgae: a method study. Arch. Hydrobiol. 121:295-306.
  3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
  4. Andreyeva, V. 1998. Terrestrial and aerophilic green algae (Chlorophyta: Terasporales, Chlorococcales, Chlorosarcinales). Nauka, St. Petersburg, 349 pp.
  5. Beers, R. F. Jr. & Sizer, I. W. 1956. Progressive inhibition of the catalase-hydrogen peroxide system by acetate, chloride and azide. Arch. Biochem. Biophys. 60:115-125. https://doi.org/10.1016/0003-9861(56)90403-9
  6. Bishoff, H. & Bold, H. C. 1963. Phycological studies. IV. Some soil algae from enchanted rock and related algae species. University of Texas Publication, Austin, TX, 95 pp.
  7. Bligh, E. G. & Dyer, W. J. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917. https://doi.org/10.1139/y59-099
  8. Borowitzka, M. 2013. Dunaliella: biology, production, and markets. In Richmond, A. & Hu, Q. (Eds.) Handbook of Microalgal Culture: Applied Phycology and Biotechnology. 2nd ed. Wiley-Blackwell, West Sussex, pp. 359-368.
  9. Borowitzka, M. A. & Moheimani, N. R. 2013. Sustainable biofuels from algae. Mitig. Adapt. Strateg. Glob. Change 18:13-25. https://doi.org/10.1007/s11027-010-9271-9
  10. Bouarab, L., Dauta, A. & Loudiki, M. 2004. Heterotrophic and mixotrophic growth of Micractinium pusillum Fresenius in the presence of acetate and glucose: effect of light and acetate gradient concentration. Water Res. 38:2706-2712. https://doi.org/10.1016/j.watres.2004.03.021
  11. Boussiba, S. 2000. Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol. Plant. 108:111-117. https://doi.org/10.1034/j.1399-3054.2000.108002111.x
  12. Brown, T. E., Richardson, F. L. & Vaughn, M. L. 1967. Development of red pigmentation in Chlorococcum wimmeri (Chlorophyta: Chlorococcales). Phycologia 6:167-184. https://doi.org/10.2216/i0031-8884-6-4-167.1
  13. Buchheim, M. A., Sutherland, D. M., Buchheim, J. A. & Wolf, M. 2013. The blood alga: phylogeny of Haematococcus (Chlorophyceae) inferred from ribosomal RNA gene sequence data. Eur. J. Phycol. 48:318-329. https://doi.org/10.1080/09670262.2013.830344
  14. 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. https://doi.org/10.3390/md12084504
  15. Chelebieva, E. S., Minyuk, G. S., Drobetskaya, I. V. & Chubchikova, I. N. 2013. Physiological and biochemical characteristics of Ettlia carotinosa Komarek 1989 (Chlorophyceae) under experimental stress condition. Mors'kyi Ekolohichnyi Zhurnal 12:78-87.
  16. Chubchikova, I. N., Minyuk, G. S. & Drobetskaya, I. V. 2010. Secondary carotenogenesis in green microalgae Scotiellopsis rubescens Vinatz. under natural insolation and temperature. Ekologiya Morya 81:77-81.
  17. Chubchikova, I. N., Minyuk, G. S., Drobetskaya, I. V. & Dantsyuk, N. V. 2009. Chlorococcal microalgae as source of natural secondary carotenoids. Ekologiya Morya 77:77-83.
  18. DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350-356. https://doi.org/10.1021/ac60111a017
  19. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. https://doi.org/10.1093/nar/gkh340
  20. Fabregas, J., Otero, A., Maseda, A. & Dominguez, A. 2001. Two-stage cultures for the production of astaxanthin from Haematococcus pluvialis. J. Biotechnol. 89:65-71. https://doi.org/10.1016/S0168-1656(01)00289-9
  21. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  22. Han, D., Li, Y. & Hu, Q. 2013. Biology and commercial aspects of Haematococcus pluvialis. In Richmond, A. & Hu, Q. (Eds.) Handbook of Microalgal Culture: Applied Phycology and Biotechnology. 2nd ed. Wiley-Blackwell, West Sussex, pp. 388-405.
  23. Hanagata, N. 1998. Phylogeny of the subfamily Scotiellocystoideae (Chlorophyceae, Chlorophyta) and related taxa inferred from 18S ribosomal RNA gene sequence data. J. Phycol. 34:1049-1054. https://doi.org/10.1046/j.1529-8817.1998.341049.x
  24. Heifetz, P. B., Forster, B., Osmond, C. B., Giles, L. J. & Boynton, J. E. 2000. Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol. 122:1439-1445. https://doi.org/10.1104/pp.122.4.1439
  25. Hoekman, S. K., Broch, A., Robbins, C., Ceniceros, E. & Natarajan, M. 2012. Review of biodiesel composition, properties, and specifications. Renew. Sustain. Energy Rev. 16:143-169. https://doi.org/10.1016/j.rser.2011.07.143
  26. Hu, C. -W., Chuang, L. -T., Yu, P. -C. & Chen, C. -N. N. 2013. Pigment production by a new thermotolerant microalga Coelastrella sp. F50. Food Chem. 138:2071-2078. https://doi.org/10.1016/j.foodchem.2012.11.133
  27. Hyka, P., Lickova, S., Přibyl, P., Melzoch, K. & Kovar, K. 2013. Flow cytometry for the development of biotechnological processes with microalgae. Biotechnol. Adv. 31:2-16. https://doi.org/10.1016/j.biotechadv.2012.04.007
  28. Islam, M. A., Magnusson, M., Brown, R. J., Ayoko, G. A., Nabi, M. N. & Heimann, K. 2013. Microalgal species selection for biodiesel production based on fuel properties derived from fatty acid profiles. Energies 6:5676-5702. https://doi.org/10.3390/en6115676
  29. Ji, F., Liu, Y., Li, G., Zhou, Y., Tian, L., Ma, Z. & Dong, R. 2013. Effects of glucose, acetic acid and glycerol on biomass accumulation of Chlorella sp. In Proc. Am. Soc. Agr. Biol. Eng. Kansas City, Missouri, 2013 July 21-24. American Society of Agricultural and Biological Engineers, St. Joseph, MI, No. 131620778.
  30. Juneja, A., Ceballos, R. M. & Murthy, G. S. 2013. Effects of environmental factors and nutrient availability on the biochemical composition of algae for biofuels production: a review. Energies 6:4607-4638. https://doi.org/10.3390/en6094607
  31. Karpagam, R., Raj, K. J., Ashokkumar, B. & Varalakshmi, P. 2015. Characterization and fatty acid profiling in two fresh water microalgae for biodiesel production: lipid enhancement methods and media optimization using response surface methodology. Bioresour. Technol. 188:177-184. https://doi.org/10.1016/j.biortech.2015.01.053
  32. Kaufnerova, V. & Elias, M. 2013. The demise of the genus Scotiellopsis Vinatzer (Chlorophyta). Nova Hedwigia 97:415-428. https://doi.org/10.1127/0029-5035/2013/0116
  33. Kobayashi, M., Kakizono, T. & Nagai, S. 1993. Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Appl. Environ. Microbiol. 59:867-873.
  34. Kessler, E. & Czygan, F. 1965. Chlorella zofingiensis Donz: Isolierung neuer Stamme und ihre physiologisch-biochemischen Eigenschaften. Ber. Deutsch. Bot. Gesell. 78:342-347.
  35. Lam, M. K. & Lee, K. T. 2011. Microalgae biofuels: a critical review of issues, problems and the way forward. Biotechnol. Adv. 30:673-690.
  36. Lemoine, Y. & Schoefs, B. 2010. Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth. Res. 106:155-177. https://doi.org/10.1007/s11120-010-9583-3
  37. Leu, S. & Boussiba, S. 2014. Advances in the production of high-value products by microalgae. Ind. Biotechnol. 10:169-183. https://doi.org/10.1089/ind.2013.0039
  38. Lichtenthaler, H. K. 1987. Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148:350-382.
  39. Liu, B. -H. & Lee, Y. -K. 2000. Secondary carotenoids formation by the green alga Chlorococcum sp. J. Appl. Phycol. 12:301-307. https://doi.org/10.1023/A:1008185212724
  40. Liu, F. J., Li, S. X., Huang, B. Q., Zheng, F. Y. & Huang, X. G. 2016. Effect of excessive $CO_2$ on physiological functions in coastal diatom. Sci. Rep. 6:21694. https://doi.org/10.1038/srep21694
  41. Lorenz, R. T. & Cysewski, G. R. 2000. Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol. 18:160-167. https://doi.org/10.1016/S0167-7799(00)01433-5
  42. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
  43. Minyuk, G. 2008. Physiological, biochemical, and biophysical characteristics of the microalga Haematococcus pluvialis, a promising source of natural astaxanthin. In Tokarev, Y. N., Finenko, Z. Z. & Shadrin, N. V. (Eds.) The Black Sea Microalgae: Problems of Biodiversity Preservation and Biotechnological Usage. ECOSI-Gidrofizika, Sevastopol, pp. 353-392.
  44. Minyuk, G. S., Chelebieva, E. S., Chubchikova, I. N., Dantsyuk, N. V., Drobetskaya, I. V., Sakhon, E. G., Chivkunova, O. B., Chekanov, K. A., Lobakova, E. S., Sidorov, R. A. & Solovchenko, A. E. 2016. pH and $CO_2$ effects on Coelastrella (Scotiellopsis) rubescens growth and metabolism. Russ. J. Plant Physiol. 63:566-574. https://doi.org/10.1134/S1021443716040105
  45. Minyuk, G. S., Drobetskaya, I. V., Chubchikova, I. N., Dantsyuk, N. V. & Chelebieva, E. S. 2010. Screening of green microalgae as potential source of nature ketocarotenoids: the relevance, strategy and study approach. Ekologiya Morya 80:67-78.
  46. Murphy, J. & Riley, J. P. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27:31-36. https://doi.org/10.1016/S0003-2670(00)88444-5
  47. Nelson, D. L. & Cox, M. M. 2013. Lehninger principles of biochemistry. 6th ed. MacMillan, New York, 1340 pp.
  48. Ozben, T. 2013. Free radicals, oxidative stress, and antioxidants: pathological and physiological significance. Vol. 296. Springer, New York, 395 рp.
  49. Pal, D., Khozin-Goldberg, I., Cohen, Z. & Boussiba, S. 2011. The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl. Microbiol. Biotechnol. 90:1429-1441. https://doi.org/10.1007/s00253-011-3170-1
  50. Perez-Perez, M. E., Lemaire, S. D. & Crespo, J. L. 2012. Reactive oxygen species and autophagy in plants and algae. Plant Physiol. 160:156-164. https://doi.org/10.1104/pp.112.199992
  51. Puncochaiova, M. & Kalina, T. 1981. Taxonomy of the genus Scotiellopsis Vinatzer (Chlorococcales, Chlorophyta). Algol. Stud. 27:119-147.
  52. Recht, L., Topfer, N., Batushansky, A., Sikron, N., Gibon, Y., Fait, A., Nikoloski, Z., Boussiba, S. & Zarka, A. 2014. Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen-starvation in the green alga Haematococcus pluvialis. J. Biol. Chem. 289:30387-30403. https://doi.org/10.1074/jbc.M114.555144
  53. Saitou, N. & Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
  54. Sarada, R., Bhattacharya, S., Bhattacharya, S. & Ravishankar, G. A. 2002. A response surface approach for the production of natural pigment astaxanthin from green alga, Haematococcus pluvialis: effect of sodium acetate, culture age, and sodium chloride. Food Biotechnol. 16:107-120. https://doi.org/10.1081/FBT-120014322
  55. Shah, M. M. R., Liang, Y., Cheng, J. J. & Daroch, M. 2016. Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Front. Plant Sci. 7:531.
  56. Singh, H., Shukla, M. R., Chary, K. V. R. & Rao, B. J. 2014. Acetate and bicarbonate assimilation and metabolite formation in Chlamydomonas reinhardtii: a $^{13}C$-NMR study. PLoS ONE 9:e106457. https://doi.org/10.1371/journal.pone.0106457
  57. Solovchenko, A. E. 2013. Physiology and adaptive significance of secondary carotenogenesis in green microalgae. Russ. J. Plant Physiol. 60:1-13. https://doi.org/10.1134/S1021443713010081
  58. Solovchenko, A. E. 2015. Recent breakthroughs in the biology of astaxanthin accumulation by microalgal cell. Photosynth. Res. 125:437-449. https://doi.org/10.1007/s11120-015-0156-3
  59. Solovchenko, A. & Chekanov, K. 2014. Production of carotenoids using microalgae cultivated in ohotobioreactors. In Paek, K. -Y., Murthy, H. N. & Zhong, J. -J. (Eds.) Production of Biomass and Bioactive Compounds Using Bioreactor Technology. Springer, Dordrecht, pp. 63-91.
  60. Solovchenko, A. & Khozin-Goldberg, I. 2013. High-$CO_2$ tolerance in microalgae: possible mechanisms and implications for biotechnology and bioremediation. Biotechnol. Lett. 35:1745-1752. https://doi.org/10.1007/s10529-013-1274-7
  61. Solovchenko, A., Merzlyak, M. N., Khozin-Goldberg, I., Cohen, Z. & Boussiba, S. 2010. Coordinated carotenoid and lipid syntheses induced in Parietochloris incisa (Chlorophyta, Trebouxiophyceae) mutant deficient in ${\Delta}$5 desaturase by nitrogen starvation and high light. J. Phycol. 46:763-772. https://doi.org/10.1111/j.1529-8817.2010.00849.x
  62. Subramanian, S., Barry, A. N., Pieris, S. & Sayre, R. T. 2013. Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production. Biotechnol. Biofuels 6:150. https://doi.org/10.1186/1754-6834-6-150
  63. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197
  64. Vonshak, A. 1985. Microalgae: laboratory growth techniques and outdoor biomass production. In Coombs, J., Hall, D. O., Long, S. P. & Scurlock, J. M. O. (Eds.) Techniques in Bioproductivity and Photosynthesis. Pergamon Press, Oxford, pp. 188-203.
  65. Wang, B., Zhang, Z., Hu, Q., Sommerfeld, M., Lu, Y. & Han, D. 2014. Cellular capacities for high-light acclimation and changing lipid profiles across life cycle stages of the green alga Haematococcus pluvialis. PLoS ONE 9:e106679. https://doi.org/10.1371/journal.pone.0106679
  66. Wiessner, W. 1979. Photoassimilation of organic compounds. In Gibbs, M. & Latzko, E. (Eds.) Encyclopedia of Plant Physiology. Springer Verlag, Berlin, pp. 181-189.
  67. Wood, A. M., Everroad, R. C. & Wingard, L. M. 2005. Measuring growth rates in microalgal cultures. In Anderson, R. A. (Ed.) Algal Culturing Techniques. Vol. 18. Elsevier Academic Press, Burlington, MA, pp. 269-288.
  68. Yu, X., Chen, L. & Zhang, W. 2015. Chemicals to enhance microalgal growth and accumulation of high-value bioproducts. Front. Microbiol. 6:56.
  69. Zhang, D. H., Ng, Y. K. & Phang, S. M. 1997. Composition and accumulation of secondary carotenoids in Chlorococcum sp. J. Appl. Phycol. 9:147-155. https://doi.org/10.1023/A:1007926528388

Cited by

  1. Nutrient Deprivation-Associated Changes in Green Microalga Coelastrum sp. TISTR 9501RE Enhanced Potent Antioxidant Carotenoids vol.17, pp.6, 2017, https://doi.org/10.3390/md17060328
  2. Revision of Coelastrella (Scenedesmaceae, Chlorophyta) and first register of this green coccoid microalga for continental Norway vol.36, pp.10, 2020, https://doi.org/10.1007/s11274-020-02897-0
  3. Adonis amurensis Is a Promising Alternative to Haematococcus as a Resource for Natural Esterified (3S,3′S)-Astaxanthin Production vol.10, pp.6, 2017, https://doi.org/10.3390/plants10061059
  4. Combined Production of Astaxanthin and β-Carotene in a New Strain of the Microalga Bracteacoccus aggregatus BM5/15 (IPPAS C-2045) Cultivated in Photobioreactor vol.10, pp.7, 2017, https://doi.org/10.3390/biology10070643
  5. Sunscreen Effect Exerted by Secondary Carotenoids and Mycosporine-like Amino Acids in the Aeroterrestrial Chlorophyte Coelastrella rubescens under High Light and UV-A Irradiation vol.10, pp.12, 2017, https://doi.org/10.3390/plants10122601