Skip to main content
SpringerLink
Log in

The Cell Ultrastructure and Autotrophic Function of the Raphidophyte Alga Heterosigma akashiwo (Y. Hada) Y. Hada ex Y. Hara and M. Chihara, 1987 under Copper Exposure

  • ORIGINAL PAPERS
  • Published:
Russian Journal of Marine Biology Aims and scope Submit manuscript

Abstract

The effect of copper (10, 25 and 50 μg/L) on the population growth, physiological state, and ultrastructure of the microalga Heterosigma akashiwo (Raphidophyceae) were studied. Copper had a greater effect on the mitochondrial membrane potential than on chlorophyll a fluorescence. The neutral lipid content was lower in the exposed cell than in control cells throughout the experiment. The morphology of organelles was not altered at any copper concentration; however, the number of vacuoles in the algal cells increased at 25 and 50 μg Cu/L.

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.

Similar content being viewed by others

REFERENCES

  1. Andreev, I.M., Role of the vacuole in the redox homeostasis of plant cells, Russ. J. Plant. Physiol., 2012, vol. 59, pp. 611–617.

    Article  CAS  Google Scholar 

  2. Zurochka, A.V., Khaidukov, S.V., Kudryavtsev, I.V., and Chereshnev, V.A., Protochnaya tsitometriya v meditsine i biologii (Flow Cytometry in Medicine and Biology), 2nd ed., Yekaterinburg: Red.-Izd. Otd., Ural. Otd. Ross. Akad. Nauk, 2014.

  3. Kachestvo morskikh vod po gidrokhimicheskim pokazatelyam. Yezhegodnik 2016 (Quality of Sea Waters Based on Hydrochemical Characteristics: Yearbook 2016), Moscow: Nauka, 2017.

  4. Orlova, T.Yu., Aizdaicher, N.A., and Stonik, I.V., Laboratornoe kul’tivirovanie morskikh mikrovodoroslei, vklyuchaya produtsentov fitotoksinov: nauchno-metodicheskoe posobie (Laboratory-Based Cultivation of Marine Microalgae, Including Producers of Phytotoxins: A Manual of Scientific Methods), Vladivostok: Dal’nauka, 2011.

  5. Solovchenko, A.E., Physiological role of neutral lipid accumulation in eukaryotic microalgae under stresses, Russ. J. Plant Physiol., 2012, vol. 59, pp. 167–176.

    Article  CAS  Google Scholar 

  6. Titov, A.F., Talanova, V.V., and Kaznina, N.M., Fiziologicheskie osnovy ustoichivosti rastenii k tyazhelym metallam: uchebnoe posobie (Physiological Bases of Heavy Metal Resistance in Plants: A Study Guide), Petrozavodsk: Inst. Biol., Karel. Nauchn. Tsentr, Ross. Akad. Nauk, 2011.

  7. Adams, M.S., Dillon, C.T., Vogt, S., et al., Copper uptake, intracellular localization and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy, Environ. Sci. Technol., 2016, vol. 50, pp. 8827–8839.

    Article  CAS  Google Scholar 

  8. Alemán-Nava, G.S., Cuellar-Bermudez, S.P., Cuaresma, M., et al., How to use Nile Red, a selective fluorescent stain for microalgal neutral lipids, J. Microbiol. Methods, 2016, vol. 128, pp. 74–79.

  9. Chen, Z., Song, S., and Wen, Y., et al., Toxicity of Cu (II) to the green alga Chlorella vulgaris: a perspective of photosynthesis and oxidant stress, Environ. Sci. Pollut. Res., 2016, vol. 23, pp. 17910−17918. https://doi.org/10.1007/s11356-016-6997-2

    Article  CAS  Google Scholar 

  10. Cid, A., Fidalgo, P., Herrero, C., and Abalde, J., Toxic action of copper on the membrane system of a marine diatom measured by flow cytometry, Cytometry, Part A, 1996, vol. 25, pp. 32–36.

    Article  CAS  Google Scholar 

  11. Cid, A., Torres, E., Herrero, C., and Abalde, J.E., Disorders provoked by copper in the marine diatom Phaeodactylum tricornutum in short-time exposure assays, Cah. Biol. Mar., 1997, vol. 38, pp. 201−206.

    Google Scholar 

  12. Dursun, F., Taş, S., and Koray, T., Spring bloom of the raphidophycean Heterosigma akashiwo in the Golden Horn Estuary at the northeast of Sea of Marmara, Ege J. Fish. Aquat. Sci., 2016, vol. 33, no. 3, pp. 201–207.

    Google Scholar 

  13. El-Naggar, A.H. and Sheikh, H.M., Response of the green microalga Chlorella vulgaris to the oxidative stress caused by some heavy metals, Life Sci. J., 2014, vol. 11, pp. 1349–1357.

    Google Scholar 

  14. Hamed, S.M., Selim, S., Klöck, G., and AbdElgawad, H., Sensitivity of two green microalgae to copper stress: Growth, oxidative and antioxidants analyses, Ecotoxicol. Environ. Saf., 2017, vol. 144, pp. 19–25.

    Article  CAS  Google Scholar 

  15. Heisler, J., Glibert, P.M., Burkholder, J.M., et al., Eutrophication and harmful algal blooms: A scientific consensus, Harmful Algae, 2008, vol. 8, pp. 3–13.

    Article  CAS  Google Scholar 

  16. Hossain, M.A., Piyatida, P., Teixeira da Silva, J.A., and Fujita, M., Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation, J. Bot., 2012, vol. 2012, art. ID 872875. https://doi.org/10.1155/2012/872875

    Article  CAS  Google Scholar 

  17. Hyka, P., Lickova, S., Přibyl, P., et al., Flow cytometry for the development of biotechnological processes with microalgae, Biotechnol. Adv., 2013, vol. 31, pp. 2–16.

    Article  CAS  Google Scholar 

  18. Kempton, J., Keppler, C.J., Lewitus, A., et al., A novel Heterosigma akashiwo (Raphidophyceae) bloom extending from a South Carolina bay to offshore waters, Harmful Algae, 2008, vol. 7, pp. 235–240.

    Article  Google Scholar 

  19. Luft, J.H., Improvements in epoxy resin embedding methods, J. Biophys. Biochem. Cytol., 1961, vol. 9, pp. 409–414.

    Article  CAS  Google Scholar 

  20. Machado, M.D. and Soares, E.V., Modification of cell volume and proliferative capacity of Pseudokirchneriella subcapitata cells exposed to metal stress, Aquat. Toxicol., 2014, vol. 147, pp. 1–6.

    Article  CAS  Google Scholar 

  21. Martínez, R., Orive, E., Laza-Martínez, A., and Seoane, S., Growth response of six strains of Heterosigma akashiwo to varying temperature, salinity and irradiance conditions, J. Plankton Res., 2010, vol. 32, pp. 529–538.

  22. Miazek, K., Iwanek, W., Remacle, C., et al., Effect of metals, metalloids and metallic nanoparticles on microalgae growth and industrial products biosynthesis: a review, Int. J. Mol. Sci., 2015, vol. 16, pp. 23929–23969.

    Article  CAS  Google Scholar 

  23. Mohamed, Z.A. and Al-Shehri, A.M., The link between shrimp farm runoff and blooms of toxic Heterosigma akashiwo in Red Sea coastal waters, Oceanologia, 2012, vol. 54, no. 2, pp. 287–309.

    Article  Google Scholar 

  24. Nagajyoti, P.C., Lee, K.D., and Sreekanth, T.V.M., Heavy metals, occurrence and toxicity for plants: a review, Environ. Chem. Lett., 2010, vol. 8, pp. 199–216.

    Article  CAS  Google Scholar 

  25. Perales-Vela, H.V., González-Moreno, S., Montes-Horcasitas, C., et al., Growth, photosynthetic and respiratory responses to sub-lethal copper concentrations in Scenedesmus incrassatulus (Chlorophyceae), Chemosphere, 2007, vol. 67, pp. 2274–2281.

    Article  CAS  Google Scholar 

  26. Pyc, M., Cai, Y., Greer, M.S., et al., Turning over a new leaf in lipid droplet biology, Trends Plant Sci., 2017, vol. 22, pp. 596–609.

    Article  CAS  Google Scholar 

  27. Reynolds, E.S., The use of lead citrate at high pH as an electron-opaque stain in electron microscopy, J. Cell Biol., 1963, vol. 17, pp. 208–212.

    Article  CAS  Google Scholar 

  28. Schmitt, F.-J., Renger, G., Friedrich, T., et al., Reactive oxygen species: Re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms, Biochim. Biophys. Acta, Bioenerg., 2014, vol. 1837, pp. 835–848.

    Article  CAS  Google Scholar 

  29. Shikata, T., Yoshikawa, S., Matsubara, T., et al., Growth dynamics of Heterosigma akashiwo (Raphidophyceae) in Hakata Bay, Japan, Eur. J. Phycol., 2008, vol. 43, pp. 395–411.

    Article  CAS  Google Scholar 

  30. Sibi, G., Anuraag, T.S., and Bafila, G., Copper stress on cellular contents and fatty acid profiles in Chlorella species, Online J. Biol. Sci., 2014, vol. 14, no. 3, pp. 209–217.

    Article  Google Scholar 

  31. Toncheva-Panova, T., Merakchiyska, M., Djingova, R., et al., Effect of Cu2+ on the red microalga Rhodella reticulata, Gen. Appl. Plant Physiol., 2006, spec. issue, pp. 53–60.

  32. Yang, J.S., Cao, J., Xing, G.L., and Yuan, H.L., Lipid production combined with biosorption and bioaccumulation of cadmium, copper, manganese and zinc by oleaginous microalgae Chlorella minutissima UTEX2341, Bioresour. Technol., 2015, vol. 175, pp. 537–544.

    Article  CAS  Google Scholar 

  33. Yruela, I., Copper in plants, Braz. J. Plant Physiol., 2005, vol. 17, pp. 145–156.

    Article  CAS  Google Scholar 

  34. Yu, J., Yang, G., and Tian, J., The effects of the harmful alga Heterosigma akashiwo on cultures of Schmackeria inopinus (Copepoda, Calanoida), J. Sea Res., 2010, vol. 64, pp. 287–294.

    Article  Google Scholar 

  35. Wang, H., Sathasivam, R., and Ki, J.-S., Physiological effects of copper on the freshwater alga Closterium ehrenbergii Meneghini (Conjugatophyceae) and its potential use in toxicity assessments, Algae, 2017, vol. 32, no. 2, pp. 131–137.

    Article  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The author thanks Miroslava A. Sabutskaya (National Scientific Center of Marine Biology FEB RAS) for her help in discussing the results of ultrastructural analysis. The culture of the microalga Heterosigma akashiwo MBRU_HAK-SR11 was provided by the Marine BioBank of the NSCMB FEB RAS (http://marbank.dvo.ru). The flow cytometric analysis was performed at the NSCMB FEB RAS. The author is sincerely grateful to the staff of the Laboratory of Cell Technologies for their help in this research.

Author information

Authors and Affiliations

  1. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041, Vladivostok, Russia

    Zh. V. Markina

Authors
  1. Zh. V. Markina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zh. V. Markina.

Ethics declarations

The author declares no conflict of interest.

This article does not contain any studies involving animals or human participants performed by the author.

Additional information

Translated by T. Koznova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Markina, Z.V. The Cell Ultrastructure and Autotrophic Function of the Raphidophyte Alga Heterosigma akashiwo (Y. Hada) Y. Hada ex Y. Hara and M. Chihara, 1987 under Copper Exposure. Russ J Mar Biol 47, 204–209 (2021). https://doi.org/10.1134/S106307402103007X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S106307402103007X

Keywords:

Search

Navigation