The Content of Primary and Secondary Carotenoids in the Cells of the Cryotolerant Microalgae Chloromonas reticulata

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Snow (cryotolerant) algae often form red (pink) spots in mountain ecosystems on snowfields around the world, but little is known about their physiology and chemical composition. The content and composition of pigments in the cells of the cryotolerant green microalgae Chloromonas reticulata have been studied. An analysis of the carotenoids content in green (vegetative) cells grown in laboratory conditions and in red resting cells collected from the snow surface in the Subpolar Urals was carried out. There were photosynthetic pigments − carotenoids such as neoxanthin, violaxanthin, anteraxanthin, zeaxanthin, lutein and β-carotene. Among the carotenoids, the ketocarotenoid astaxanthin, which has a high biological activity, was also found. It was established that the cultivation of algae at low positive temperature (+6 °C) and moderate illumination (250 μmol quanta/(m2⋅s) contributed to the accumulation of all identified carotenoids, including extraplastidic astaxanthin. In addition to the pigments, fatty acids accumulated in the algae cells. The data obtained allow us to consider the studied microalgae as a potentially promising species for the production of carotenoids.

Full Text

Restricted Access

About the authors

O. V. Dymova

Institute of Biology of the Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Author for correspondence.
Email: dymovao@ib.komisc.ru
Russian Federation, Syktyvkar

V. S. Parshukov

Institute of Biology of the Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Email: dymovao@ib.komisc.ru
Russian Federation, Syktyvkar

I. V. Novakovskaya

Institute of Biology of the Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Email: dymovao@ib.komisc.ru
Russian Federation, Syktyvkar

E. N. Patova

Institute of Biology of the Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Email: dymovao@ib.komisc.ru
Russian Federation, Syktyvkar

References

  1. Hoffmann, L. (1989) Algae of terrestrial habitats, Bot. Rev., 55, 77-105.
  2. AlgaeBase. In World-Wide Electronic Publication; National University of Ireland: Galway, Ireland, 2023, URL: https://www.algaebase.org.
  3. Masojídek, J., Torzillo, G., and Koblížek, M. (2013) Photosynthesis in microalgae, in Handbook of Microalgal Culture: Applied Phycology and Biotechnology, 2nd ed (Richmond, A., and Hu, Q., eds) Chichester, Wiley-Blackwell, Chap. 2, pp. 21-35, https://doi.org/10.1002/9781118567166.ch2.
  4. Borowitzka, M. A. (2013) High-value products from microalgae – their development and commercialisation, J. Appl. Phycol., 25, 743-756, https://doi.org/10.1007/s10811-013-9983-9.
  5. 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, 229-242, https://doi.org/10.1111/jpy.12173.
  6. 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.
  7. Puchkova, T. V., Khapchaeva, S. A., Zotov, V. S., Lukyanov, A. A., and Solovchenko, A. E. (2021). Marine and freshwater microalgae as sustainable source cosmeceuticals, Marine Biol. J., 6, 67-81, https://doi.org/10.21072/mbj.2021.06.1.06.
  8. Chen, H., Qiu, T., Rong, J., He, C., and Wang, Q. (2015) Microalgal biofuel revisited: an informatics-based analysis of developments to date and future prospects, Appl. Energy, 155, 585-598, https://doi.org/10.1016/ wj.apenergy.2015.06.055.
  9. Vecchi, V., Barera, S., Bassi, R., and Dall’Osto, L. (2020) Potential and challenges of improving photosynthesis in Algae, Plants, 9, 67, https://doi.org/10.3390/plants9010067.
  10. Remias, D., Lütz-Meindl, U., and Lütz, C. (2005) Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis, Eur. J. Phycol., 40, 259-268, https://doi.org/10.1080/09670260500202148.
  11. Prochazkova, L., Remias, D., Holzinger, A., Resanka, T., and Nedbalova, L. (2021) Ecophysiological and ultrastructural characterisation of the circumpolar orange snow alga Sanguina aurantia compared to the cosmopolitan red snow alga Sanguina nivaloides (Chlorophyta), Polar Biol., 44, 105-117, https://doi.org/10.1007/s00300020-02778-0.
  12. Holzinger, A., and Karsten, U. (2013) Dessication stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms, Front. Plant Sci., 4, 327, https://doi.org/10.3389/fpls. 2013.00327.
  13. Gong, M., and Bassi, A. (2016) Carotenoids from microalgae: a review of recent developments, Biotechnol. Adv., 34, 1396-1412, https://doi.org/10.1016/j.biotechadv.2016.10.005.
  14. Yang, Y., Seo, J. M., Nguyen, A., Pham, T. X., Park, H. J., Park, Y., Kim, B., Bruno, R. S., and Lee, J. (2011) Astaxanthin rich extract from the green alga Haematococcus pluvialis lowers plasma lipid concentrations and enhances antioxidant defense in apolipoprotein E knockout mice, J. Nutr., 141, 1611-1617, https://doi.org/10.3945/jn.111.142109.
  15. Minyuk, G., Chelebieva, E., Chubchikova, I., Dantsyuk, N., Drobetskaya, I., Sakhon, E., Chekanov, K., and Solovchenko, A. (2017) Stress-induced secondary carotenogenesis in Coelastrella rubescens (Scenedesmaceae, Chlorophyta), a producer of value-added keto-carotenoids, Algae, 32, 245-259, https://doi.org/10.4490/algae.2017.32.8.6.
  16. Singh, D. P., Khattar, J. S., Rajput, A., Chaudhary, R., and Singh, R. (2019) High production ofcarotenoids by the green microalga Asterarcys quadricellulare PUMCC 5.1.1 under optimized culture conditions, PLoS One, 14, e0221930, https://doi.org/10.1371/journal.pone.0221930.
  17. Chekanov, K., Fedorenko, T., Kublanovskaya, A., Litvinov, D., and Lobakova, E. (2019) Diversity of carotenogenic microalgae in the White Sea polar region, FEMS Microbiol. Ecol., 96, fiz183, https://doi.org/10.1093/ femsec/fiz183.
  18. Wang, B., Zarka, A., Trebst, A., and Boussiba, S. (2003) Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance, J. Phycol., 39, 1116-1124, https://doi.org/10.1111/j.0022-3646.2003.03-043.x.
  19. Christaki, E., Bonos, E., Giannenas, I., and Florou-Paneri, P. (2013) Functional properties of carotenoids originating from algae, J. Sci. Food Agric., 93, 5-11, https://doi.org/10.1002/jsfa.5902.
  20. Palozza, P., and Krinsky, N. I. (1992) Astaxanthin and canthaxanthin are potent antioxidants in a membrane model, Arch. Biochem. Biophys., 297, 291-295, https://doi.org/10.1016/0003-9861(92)90675-m.
  21. Lorenz, R. T., and 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.
  22. Guerin, M., Huntley, M., and Olaizola, M. (2003) Haematococcus astaxanthin: applications for human health and nutrition, Trends Biotechnol., 21, 210-216, https://doi.org/10.1016/S0167-7799(03)00078-7.
  23. Naguib, Y. (2000) Antioxidant activities of astaxanthin and related carotenoids, J. Agric. Food Chem., 48, 1150-1154, https://doi.org/10.1021/jf991106k.
  24. Lemoine, Y., and 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.
  25. Boussiba, S. (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response, Physiol. Planth., 108, 111-117, https://doi.org/10.1034/j.1399-3054.2000.108002111.x.
  26. Williams, W. E., Gorton, H. L., and Vogelmann, T. C. (2003) Surface gas-exchange processes of snow algae, Proc. Natl. Acad. Sci. USA, 100, 562-566, https://doi.org/10.1073/pnas.02355601.
  27. Hoham, R. W., Berman, J. D., Rogers, H. S., Felio, J. H., Ryba, J. B. and Miller, P. R. (2006) Two new species of green snow algae from Upstate New York, Chloromonas chenangoensis sp. nov. and Chloromonas tughillensis sp. nov. (Volvocales, Chlorophyceae) and the effects of light on their life cycle development, Phycologia, 45, 319-330, https://doi.org/10.2216/04-103.1.
  28. Hoham, R. W., and Remias, D. (2020) Snow and glacial algae: a review, J. Phycol., 56, 264-282, https://doi.org/ 10.1111/jpy.12952.
  29. Zheng, Y., Xue, C., Chen, H., He, C., and Wang, Q. (2020) Low-temperature adaptation of the snow alga Chlamydomonas nivalis is associated with the photosynthetic system regulatory process, Front. Microbiol., 11, 1233, https://doi.org/10.3389/fmicb.2020.01233.
  30. Suzuki, P., Detain, A., Park, Y., Viswanath, K., Wijffels, R. H., Leborgne-Castel, N., Procházková, L., Hulatt, C. J. (2023) Phylogeny and lipid profiles of snow-algae isolated from Norwegian red-snow microbiomes, FEMS Microbiol. Ecol., 99, 1-18, https://doi.org/10.1093/femsec/fiad057.
  31. Новаковская И. В., Патова Е. Н., Макеева Е. Г. (2022) Снежные водоросли и цианобактерии ряда районов Урала и Западного Саяна, Теор. Прикл. Экол., 3, 149-156, https://doi.org/10.25750/1995-4301-2022-3-149-156.
  32. Novakovskaya, I. V., Patova, E. N., Boldina, O. N., Patova, A. D., and Shadrin D. M. (2018) Molecular phylogenetic analyses, ecology and morphological characteristics of Chloromonas reticulata (Goroschankin) Gobi which causes red blooming of snow in the Subpolar Urals, Cryptogamie, Algologie, 39, 199-213, https://doi.org/10.7872/ crya/v39.iss2.2018.199.
  33. Stanier, R., Kunisawa, R., Mandel M., and Cohen-Bazire G. (1971) Purification and properties of unicellular blue–green algae (order Chroococcales), Bacteriol. Rev., 35, 171-205, https://doi.org/10.1128/br.35.2.171-205.1971.
  34. Andersen, R. A. (2005) Algal Culturing Techniques, Elsevier, New York, NY, USA, pp. 589.
  35. Droop, M. R. (1955) Carotenogenesis in Haematococcus pluvialis, Nature, 175, 42, https://doi.org/10.1038/175042A0.
  36. Procházková, L., Leya, T., Křížková, H., and Nedbalová, L. (2019) Sanguina nivaloides and Sanguina aurantia gen. et spp. nov. (Chlorophyta): the taxonomy, phylogeny, biogeography and ecology of two newly recognized algae causing red and orange snow, FEMS Microbiol. Ecol., 95, fiz064, https://doi.org/10.1093/femsec/fiz064.
  37. Dymova, O., Khrystin, M., Miszalski, Z., Kornas, A., Strzalka, K., and Golovko, T. (2018) Seasonal variations of leaf chlorophyll–protein complexes in the wintergreen herbaceous plant Ajuga reptans L., Func. Plant Biol., 45, 519-527, https://doi.org/10.1071/FP17199.
  38. Chekanov, K., Lobakova, E., Selyakh, I., Semenova, L., Sidorov, R., and 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.
  39. Chekanov, K., Litvinov, D., Fedorenko, T., Chivkunova, O., and Lobakova, E. (2021) Combined production of astaxanthin and β-carotene in a new strain of the microalga Bracteacoccus aggregatus BM5/15 (IPPAS C-2045) cultivated in photobioreactor, Biology, 10, 643, https://doi.org/10.3390/biology10070643.
  40. Corato, A., Le, T. T., Baurain, D., Jacques, P., Remacle, C., and Franck, F. A. (2022) Fast-growing oleaginous strain of Coelastrella capable of astaxanthin and canthaxanthin accumulation in phototrophy and heterotrophy, Life, 12, 334, https://doi.org/10.3390/life12030334.
  41. Opinion of the Scientific Panel on additives and products or substances used in animal feed (FEEDAP) on the safety of use of colouring agents in animal nutrition – PART I. General Principles and Astaxanthin, (2005), EFSA J., 291, 1-40, URL: https://www.efsa.europa.eu/en/efsajournal/pub/291.
  42. Kobayashi, M., Kakizono, T., Yamaguchi, K., Nishio, N., and Nagai, S. (1992) Growth and astaxanthin formation of Haematococcus pluvialis in heterotrophic and mixotrophic conditions, J. Ferment. Bioeng., 74, 17-20, https://doi.org/10.1016/0922-338X(92)90261-R.
  43. Ben-Amotz, A., Katz, A., and Avron, M. (1982) Accumulation of β-carotene in halotolerant algae: purification and characterization of β-carotene rich globules from Dunaliella bardawil (Chlorophycea), J. Phycol., 18, 529-537, https://doi.org/10.1111/j.1529-8817.1982.tb03219.x.
  44. Grung, M., D’Souza, F. M. L., Borowitzka, M., and Liaaen-Jensen, S. (1992) Algal Carotenoids 51. Secondary Carotenoids 2. Haematococcus pluvialis aplanospores as a source of (3S, 3′S)-astaxanthin esters, J. Appl. Phycol., 4, 165-171, https://doi.org/10.1007/BF02442465.
  45. Czygan, F. (1970) Blood-rain and blood-snow: nitrogen-deficient cells of Haematococcus pluvialis and Chlamydomonas nivalis, Arch. Mikrobiol., 74, 69-76, https://doi.org/10.3354/meps08849.
  46. Челебиева Э. С. (2014) Особенности вторичного каротиногенеза у зеленых микроводорослей, Автореф. дис. канд. биол. наук, Институт биологии южных морей, Севастополь.
  47. Bishop, N.I., Bulga, B., and Senger, H. (1998) Photosynthetic capacity and quantum requirement of three secondary mutants of Scenedesmus obliquus with deletions in carotenoid biosynthesis, Bot. Acta., 111, 231-235, https://doi.org/10.1111/j.1438-8677.1998.tb00700.x.
  48. Polle, J. E., Niyogi, K. K., and Melis, A. (2001) Absence of lutein, violaxanthin and neoxanthin affects the functional chlorophyll antenna size of photosystem-II but not that of photosystem-I in the green alga Chlamydomonas reinhardtii, Plant Cell Physiol., 42, 482-491, https://doi.org/10.1093/pcp/pce058.
  49. Morgan-Kiss, R. M., Priscu, J. C., Pocock, T., Gudynaite-Savitch, L., and Huner, N. P. A (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments, Microbiol. Mol. Biol. R, 70, 222-252, https://doi.org/10.1128/MMBR.70.1.222-252.2006.
  50. Spijkerman, E., Wacker, A., Weithoff, G., and Leya, T. (2012) Elemental and fatty acid composition of snow algae in Arctic habitats, Front. Microbiol., 3, 380, https://doi.org/10.3389/fmicb.2012.00380.
  51. Demmig-Adams, B., and Adams, W. W. (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis, Trends Plant Sci., 1, 21-26, https://doi.org/10.1016/S1360-1385(96)80019-7.
  52. Bidigare, R. R., Ondrusek, M. E., Kennicutt II, M. C., Iturriaga, R., Harvey, H. R., Hohan, R. W., and Macko S. A. (1993) Evidence for photoprotective function for secondary carotenoids of snow algae, J. Phycol., 29, 427-434, https://doi.org/10.1111/j.1529-8817.1993.tb00143.x.
  53. Соловченко А. Е., Мерзляк М. Н. (2008) Экранирование видимого и УФ излучения как фотозащитный механизм растений, Физиол. Раст., 55, 803-822.
  54. Rau, W. (1988) Functions of carotenoids other than in photosynthesis, in Plant Pigments (Goodween, T. W., ed) Academic Press, London, pp. 231-255.
  55. Gu, W., Li, H., Zhao, P., Yu, R., Pan, G., Gao, S., Xie, X., Huang, A., He, L., and Wang, G. (2014) Quantitative proteomic analysis of thylakoid from two microalgae (Haematococcus pluvialis and Dunaliella salina) reveals two different high light-responsive strategies, Sci. Rep., 4, 1-12, https://doi.org/10.1038/srep06661.

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Cells of the alga Chloromonas reticulata and cells collected from the surface of stained snow in the Subpolar Urals: a - mobile cell of C. reticulata with flagella, scale bar - 10 µm; b - vegetative cells of C. reticulata; scale bar - 10 µm; old cells of C. reticulata with flagella, scale bar - 10 µm; b - vegetative cells of C. reticulata, scale bar - 10 µm; c - old cells of C. reticulata, scale bar - 10 µm; d - red cells collected from snow surface, scale bar - 10 µm. Photo by I.V. Novakovskaya

Download (320KB)
3. Fig. 2. Scheme of the installation. 1 - compressor; 2 - connecting tube; 3 - flask with water; 4 - flask with microalgae; 5 - light sources: LED-A60-15W/SPSB/E27/CL PLP30WH 50 µmol/(m2⋅s) and LED-A60-15W/SPSB/E27/CL PLP30GR (China) 250 µmol/(m2⋅s) lamps

Download (51KB)
4. Fig. 3. Elution profile during HPLC separation of pigments extracted from vegetative (green) cells of Chloromonas reticulata. Variants: a - low temperature and light 50 µmol/(m2⋅s); b - low temperature and light 250 µmol/(m2⋅s). Pigments: Neo, neoxanthin; Vio, violaxanthin; Ast, astaxanthin; Ant, anteraxanthin; Lut, lutein; Zea, zeaxanthin; β-car, β-carotene; Chl a, chlorophyll a; Chl b, chlorophyll b. Detection was performed by recording the absorbance of the mobile phase at 440 nm

Download (91KB)
5. Fig. 4. Elution profile of HPLC separation of pigments extracted from resting (red) cells of Chloromonas reticulata. The other notations are as in Fig. 3

Download (73KB)

Copyright (c) 2024 Russian Academy of Sciences