Skip to main content
SpringerLink
Log in

Characteristics of a New Halotolerant Arctic Strain of Carotenogenic Microalga Halochlorella rubescens NAMSU SBB-20

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Green microalgae capable of accumulating secondary carotenoids are the most important objects of biotechnology, and the search for new strains with unique properties, in particular, those adapted to growth at low temperatures and high salinity in the environment, is an urgent task. The NAMSU SBB-20 microalga strain was isolated from an algal-bacterial biofilm found on the coast of the White Sea in the littoral zone of the Solovetsky Archipelago. Identification of the strain showed its belonging to the species Halochlorella rubescens P.J.L.Dangeard. The species H. rubescens was first described for the White Sea. Under conditions of high light intensity, ultrastructural changes in cells are shown, among which destruction of the photosynthetic apparatus and the formation of cytoplasmic and chloroplast lipid inclusions are noted. It was shown that the culture of the NAMSU SBB-20 strain is capable of acquiring an orange color under unfavorable growth conditions. An assessment was made of the effect of the composition of the medium and the intensity of illumination on the pigment composition of the algae. The highest absolute values of the accumulation of carotenoids were noted during cultivation in light with an intensity of 150 μmol PAR quanta/m2/s on BG-11 media containing no source of phosphorus (15.66 ± 0.18 mg/L) or nitrogen (15.95 ± 0.56 mg/L). The described strain has a biotechnological potential due to the initial halotolerance and the accumulation of high values of secondary carotenoids in the biomass.

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.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Borowitzka, M.A., Commercial production of microalgae: ponds, tanks, tubes and fermenters, J. Biotechnol., 1999, vol. 70, nos. 1–3, p. 313. https://doi.org/10.1016/S0168-1656(99)00083-8

    Article  CAS  Google Scholar 

  2. Guerin, M., Huntley, M., and Olaizola, M., Haematococcus astaxanthin: applications for human health and nutrition, Trends Biotechnol., 2003, vol. 21, no. 5, p. 210. https://doi.org/10.1016/S0167-7799(03)00078-7

    Article  CAS  PubMed  Google Scholar 

  3. Solovchenko, A. and Chekanov, K., Production of carotenoids using microalgae cultivated in photobioreactors, Production of Biomass and Bioactive Compounds Using Bioreactor Technology, Paek, K.Y., Murthy, H., and Zhong, J., Eds., Dordrecht: Springer, 2014, p. 63. https://doi.org/10.1007/978-94-017-9223-3_4

    Book  Google Scholar 

  4. Chekanov, K., Fedorenko, T., Kublanovskaya, A., Litvinov, D., and Lobakova, E., Diversity of carotenogenic microalgae in the White Sea polar region, FEMS Microbiol. Ecol., 2020, vol. 96, p. 183. https://doi.org/10.1093/femsec/fiz183/5632105

    Article  Google Scholar 

  5. Stanier, R., Kunisawa, R., Mandel, M., and Cohen-Bazire, G., Purification and properties of unicellular blue-green algae (order Chroococcales), Bacteriol. Rev., 1971, vol. 35, p. 171. https://doi.org/10.1128/br.35.2.171-205.1971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Temraleeva, A.D., Mincheva, E.V., Bukin, Yu.S., and Andreeva, A.M., Sovremennye metody vydeleniya, kul’tivirovaniya i identifikatsii zelenykh vodorosley (Chlorophyta) (Modern Methods of Isolation, Cultivation and Identification of Green Algae (Chlorophyta)), Kostroma: Kostromskoy pechatnyy dom, 2014.

  7. Wang, Y., Tian, R.M., Gao, Z.M., Bougouffa, S., and Qian, P.Y., Optimal eukaryotic 18S and universal 16S/18S ribosomal RNA primers and their application in a study of symbiosis, PloS One, 2014, vol. 9, no. 3, p. e90053. https://doi.org/10.1371/journal.pone.0090053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ismagulova, T., Chekanov, K., Gorelova, O., Baulina, O., Semenova, L., Selyakh, I., Chivkunova, O., Lobakova, E., Karpova, O., and Solovchenko, A., A new subarctic strain of Tetradesmus obliquus—part I: identification and fatty acid profiling, J. Appl. Phycol., 2018, vol. 30, no. 5, p. 2737. https://doi.org/10.1007/s10811-017-1313-1

    Article  CAS  Google Scholar 

  9. Maltsev, Y., Gusev, E., Maltseva, I., Kulikovskiy, M., Namsaraev, Z., Petrushkina, M., Filimonova, A., Sorokin, B., Golubeva, A., Butaeva, G., Khrushchev, A., Zotko, N., and Kuzmin, D., Description of a new species of soil algae, Parietochloris grandis sp. nov., and study of its fatty acid profiles under different culturing conditions, Algal Res., 2018, vol. 33, p. 358. https://doi.org/10.1016/j.algal.2018.06.008

    Article  Google Scholar 

  10. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res., 1997, vol. 25, no. 17, p. 3389. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Edgar, G.J., Stuart-Smith, R.D., Willis, T.J., Kininmonth, S., Baker, S.C., Banks, S., and Thomson, R.J., Global conservation outcomes depend on marine protected areas with five key features, Nature, 2014, vol. 506, no. 7487, p. 216.

    Article  CAS  PubMed  Google Scholar 

  12. Kumar, S., Stecher, G., and Tamura, K., MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, p. 1870. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Aldrich, J., RA Fisher and the making of maximum likelihood 1912-1922, Stat Sci., 1997, vol. 12, no. 3, p. 162. https://doi.org/10.1214/ss/1030037906

    Article  Google Scholar 

  14. Kimura, M., A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol., 1980, vol. 16, no. 2, p. 111. https://doi.org/10.1007/BF01731581

    Article  CAS  PubMed  Google Scholar 

  15. Nei, M. and Kumar, S., Molecular Evolution and Phylogenetics, Oxford: Oxford University Press, 2000.

    Google Scholar 

  16. Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 1985, vol. 39, no. 4, p. 783. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Article  PubMed  Google Scholar 

  17. Gorelova, O., Baulina, O., Solovchenko, A., Selyakh, I., Chivkunova, O., Semenova, L., Scherbakov, P., Burakova, O., and Lobakova, E., Coordinated rearrangements of assimilatory and storage cell compartments in a nitrogen-starving symbiotic chlorophyte cultivated under high light, Arch. Microbiol., 2015, vol. 197, p. 181. https://doi.org/10.1007/s00203-014-1036-5

    Article  CAS  PubMed  Google Scholar 

  18. Reynolds, E., The use of lead citrate at high pH as an electron-opaque stain in electron microscopy, J. Cell Biol., 1963, vol. 17, no. 1, p. 208. https://doi.org/10.1083/jcb.17.1.208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Anderson, T.F., Techniques for the preservaation of three-dimensional structure in preparing specimens for the electron microscope, Trans. N.Y. Acad. Sci., 1951, vol. 13, no. 4, p. 130. https://doi.org/10.1111/j.2164-0947.1951.tb01007.x

    Article  Google Scholar 

  20. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., and Stanier, R.Y., Generic assignments, strain histories and properties of pure cultures of cyanobacteria, Microbiology, 1979, vol. 111, no. 1, p. 1. https://doi.org/10.1099/00221287-111-1-1

    Article  Google Scholar 

  21. Solovchenko, A., Merzlyak, M.N., 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, no. 4, p. 763. https://doi.org/10.1111/j.1529-8817.2010.00849.x

    Article  CAS  Google Scholar 

  22. Guiry, M.D. and Guiry, G.M., AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. https://www.algaebase.org. Accessed November 26, 2022.

  23. Kessler, E., Schäfer, M., Hümmer, C., Kloboucek, A., and Huss, V.A.R., Physiological, biochemical, and molecular characters for taxonomy of the subgenera of Scenedesmus (Chlorococcales, Chlorophyta), Bot. Acta, 1997, vol. 110, p. 244. https://doi.org/10.1111/j.1438-8677.1997.tb00636.x

    Article  Google Scholar 

  24. Kessler, E., Czygan, F.C., Fott, B., and Nováková, M., Über Halochlorella rubescens Dangeard, Protistenk, 1968, vol. 110, p. 462.

    Google Scholar 

  25. Kalina, T. and Puncochárová, M., Taxonomy of the subfamily Scotiellocystoideae Fott 1976 (Chlorellaceae, Chlorophyceae), Archiv für Hydrobiologie. Supplementband. Monographische Beiträge, 1987, vol. 73, no. 4, p. 473.

    Google Scholar 

  26. Huss, V.A., Frank, C., Hartmann, E.C., Hirmer, M., Kloboucek, A., Seidel, B.M., Wenzeler, P., and Kessler, E., Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta), J. Phycol., 1999, vol. 35, no. 3, p. 587. https://doi.org/10.1046/j.1529-8817.1999.3530587.x

    Article  CAS  Google Scholar 

  27. Chesunov, A.V., Kalyakina, N.M., and Bubnova, E.N., Katalog bioty Belomorskoy biologicheskoy stantsii MGU (Biota Catalog of the White Sea Biological Station of Moscow State University), Moscow: Tov. Nauch. Izd. KMK, 2008.

  28. Shi, J., Podola, B., and Melkonian, M., Application of a prototype-scale Twin-Layer photobioreactor for effective N and P removal from different process stages of municipal wastewater by immobilized microalgae, Biores. Technol., 2014, vol. 154, p. 260. https://doi.org/10.1016/j.biortech.2013.11.100

    Article  CAS  Google Scholar 

  29. Jo, S.W., Hong, J.W., Do, J.M., Na, H., Kim, J.J., Park, S.I., Kim, Y.S., Kim, I.S., and Yoon, H.S., Nitrogen deficiency-dependent abiotic stress enhances carotenoid production in indigenous green microalga Scenedesmus rubescens KNUA042, for use as a potential resource of high value products, Sustainability, 2020, vol. 12, no. 13, p. 5445. https://doi.org/10.3390/su12135445

    Article  CAS  Google Scholar 

  30. Tsavatopoulou, V.D., Aravantinou, A.F., Vakros, J., and Manariotis, I.D., Conversion of Scenedesmus rubescens lipid into biodiesel by biochar of different origin, Catalysts, 2021, vol. 11, no. 9, p. 1116. https://doi.org/10.3390/catal11091116

    Article  CAS  Google Scholar 

  31. Zaytseva, A., Chekanov, K., Zaytsev, P., Bakhareva, D., Gorelova, O., Kochkin, D., and Lobakova, E., Sunscreen effect exerted by secondary carotenoids and mycosporine-like amino acids in the aeroterrestrial chlorophyte Coelastrella rubescens under high light and UV-A irradiation, Plants, 2021, vol. 10, no. 12, p. 2601. https://doi.org/10.3390/plants10122601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Solovchenko, A.E., Physiological role of neutral lipid accumulation in eukaryotic microalgae under stresses, Russ. J. Plant Physiol., 2012, vol. 59, no. 2, p. 167. https://doi.org/10.1134/S1021443712020161

    Article  CAS  Google Scholar 

  33. Davidi, L., Shimoni, E., Khozin-Goldberg, I., Zamir, A., and Pick, U., Origin of β-carotene-rich plastoglobuli in Dunaliella bardawil, Plant Physiol., 2014, vol. 164, no. 4, p. 2139. https://doi.org/10.1104/pp.113.235119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ota, S., Morita, A., Ohnuki, S., Hirata, A., Sekida, S., Okuda, K., Ohya, Y., and Kawano, S., Carotenoid dynamics and lipid droplet containing astaxanthin in response to light in the green alga Haematococcus pluvialis, Sci. Rep., 2018, vol. 8, no. 1, p. 1. https://doi.org/10.1038/s41598-018-23854-w

    Article  CAS  Google Scholar 

  35. Chekanov, K., Litvinov, D., Fedorenko, T., Chivkunova, O., and Lobakova, E., 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, 2021, vol. 10, no. 7, p. 643. https://doi.org/10.3390/biology10070643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

ACKNOWLEDGMENTS

We are grateful to Professor of the Department of Bioengineering, Faculty of Biology, Moscow State University, Dr.Bio.Sci. A.E. Solovchenko for help in interpreting some of the results. Electron microscopic studies were carried out using the equipment of the Center for Collective Use of Moscow State University.

Funding

This work was supported by a grant from the president of the Russian Federation (no. MK-1952.2021.1.4) as well as by the Molecular Technologies of Living Systems and Synthetic Biology Scientific and Educational School of Moscow State University.

Author information

Authors and Affiliations

  1. Moscow State University, Moscow, Russia

    A. A. Zaitseva, D. A. Bakhareva, P. A. Zaitsev & E. S. Lobakova

Authors
  1. A. A. Zaitseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. A. Bakhareva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. A. Zaitsev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. S. Lobakova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Zaitseva.

Ethics declarations

This article does not contain any studies involving humans and animals as subjects. The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zaitseva, A.A., Bakhareva, D.A., Zaitsev, P.A. et al. Characteristics of a New Halotolerant Arctic Strain of Carotenogenic Microalga Halochlorella rubescens NAMSU SBB-20. Russ J Plant Physiol 70, 49 (2023). https://doi.org/10.1134/S1021443722603123

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1134/S1021443722603123

Keywords:

Search

Navigation