Skip to main content
Log in

The Impact of Temperature Stress on DNA and RNA Synthesis in Potentially Toxic Dinoflagellates Prorocentrum minimum

  • Comparative and Ontogenic Physiology
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

Biomarkers of temperature stress were studied as major characteristics crucial for the understanding complex processes that underlie the response of marine planktonic microorganisms to environmental factors and their sublethal effects. Using the potentially toxic dinoflagellates Prorocentrum minimum as a model object, the impact of temperature stress on viability, cell cycle, RNA synthesis and DNA replication in these protists was evaluated. It was shown by flow cytometry that stress evoked by a temperature increase from 25°C (control) to 37 or 42°C during 15 to 60 min did not cause any considerable alterations in the cell cycle, while cell death rate increased from ≤ 1% (control) to 2–12% at 37°C and 4–22% at 42°C. Along with a relatively low cell death rate, following a temperature increase to 37 and/or 42°C, P. minimum displayed the ability to boost the synthesis of DNA (1.7–1.9 and 1.2–1.6 times, respectively) and especially RNA (2.5–3.1 and 1.7–2.8 times, respectively) during the first 15–30 min after stress. At certain stages of the life cycle, this effect can be critical for maintaining the viability and normal development of the P. minimum population. The obtained results demonstrate that a significantly elevated synthesis of nucleic acids can serve as an indicator (biomarker) of sublethal environmental stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Okolodkov, Yu.B., Dinoflagellata, Protisty. Rukovodstvo po zoologii (Protists. Handbook for Zoology), 2011, Moscow, pp. 7–94.

    Google Scholar 

  2. Hallegraeff, G.M., A review of harmful algal blooms and their apparent global increase, Phycol., 1993, vol. 32, no. 2, pp. 79–99.

    Article  Google Scholar 

  3. Hackett, J.D., Anderson, D.M., Erdner, D.L., and Bhattacharya, D., Dinoflagellates: a remarkable evolutionary experiment, Am. J. Bot., 2004, vol. 91, pp. 1523–1534.

    Article  CAS  PubMed  Google Scholar 

  4. Telesh, I.V., Schubert, H., and Skarlato, S.O., Ecological niche partitioning of the invasive dinoflagellate Prorocentrum minimum and its native congeners in the Baltic Sea, Harmful Algae, 2016, vol. 59, pp. 100–111.

    Article  CAS  PubMed  Google Scholar 

  5. Skarlato, S.O. and Telesh, I.V., Development of the protistan species-maximum concept for the critical salinity zone, Russ. J. Mar. Biol., 2017, vol. 43, no 1, pp. 1–11.

    Article  Google Scholar 

  6. Orlova, T.Y., Konovalova, G.V., Stonik, I.V., Selina, M.S., Morozova, T.V., and Shevchenko, O.G., Harmful algal blooms on the eastern coast of Russia, PICES Sci. Rep., 2014, vol. 47, pp. 41–58.

    Google Scholar 

  7. Wasmund, N., Göbel, J., and Bodungen, B.V., 100-years-changes in the phytoplankton community of Kiel Bight (Baltic Sea), J. Mar. Syst., 2008, vol. 73, pp. 300–322.

    Article  Google Scholar 

  8. Glibert, P.M., Azanza, R., Burford, M., Furuya, K., Abal, E., et al., Ocean urea fertilization for carbon credits poses high ecological risks, Mar. Pollut. Bull., 2008, vol. 56, pp. 1045–1056.

    Article  CAS  Google Scholar 

  9. Olenina, I., Wasmund, N., Hajdu, S., Jurgensone, I., Gromisz, S., Kownacka, J., Toming, K., Vaiciute, D., and Olenin, S., Assessing impacts of invasive phytoplankton: The Baltic Sea case, Mar. Pollut. Bull., 2010, vol. 60, pp. 1691–1700.

    Article  CAS  PubMed  Google Scholar 

  10. Hajdu, S., Edler, L., Olenina, I., and Witek, B., Spreading and establishment of the potentially toxic dinoflagellate Prorocentrum minimum in the Baltic Sea, Int. Rev. Hydrobiol., 2000, vol. 85, pp. 561–575.

    Article  Google Scholar 

  11. Hajdu, S., Pertola, S., and Kuosa, H., Prorocentrum minimum (Dinophyceae) in the Baltic Sea: morphology, occurrence–a review, Harmful Algae, 2005, vol. 4, pp. 471–480.

    Article  CAS  Google Scholar 

  12. Grzebyk, D. and Berland, B., Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae), Mediter. Sea J. Plankton Res., 1996, vol. 18, pp. 1837–1849.

    Article  Google Scholar 

  13. Pertola, S., Kuosa, H., and Olsonen, R., Is the invasion of Prorocentrum minimum (Dinophyceae) related to the nitrogen enrichment of the Baltic Sea? Harmful Algae, 2005, vol. 4, pp. 481–492.

    Article  CAS  Google Scholar 

  14. Werner, I., Stephen, L.C., and Hinton, D.E., Biomarkers aid understanding of aquatic organism responses to environmental stressors, Calif. Agr., 2003, vol. 57, no. 4, pp. 110–115.

    Article  Google Scholar 

  15. Rizzo, P.J., The enigma of the dinoflagellate chromosome, J. Protozool., 1991, vol. 38, pp. 246–252.

    Article  Google Scholar 

  16. Moustafa, A., Evans, A.N., Kulis, D.M., Hackett, J.D., Erdner, D.L., Anderson, D.M., and Bhattacharya, D., Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence, PLoS ONE, vol. 5. https://doi.org/10.1371/journal.pone.0009688

  17. Skarlato, S., Filatova, N., Knyazev, N., Berdieva, M., and Telesh, I., Salinity stress response of the invasive dinoflagellate Prorocentrum minimum, Estuar. Coast. Shelf Sci., 2017. http://dx.doi.org/10.1016/j.ecss.2017.07.007

    Google Scholar 

  18. Spector, D.L., Dinoflagellate nuclei, Dinoflagellates, Spector, D.L., Ed., Orlando, USA, 1984, pp. 107–147.

  19. Hackett, J.D., Scheetz, T.E., Yoon, H.S., Soares, M.B., Bonaldo, M.F., Casavant, T.L., and Bhattacharya, D., Insights into a dinoflagellate genome through expressed sequence tag analysis, BMC Genomics, 2005, vol. 6: e80. https://doi.org/10.1186/1471-2164-6-80.

    Article  Google Scholar 

  20. Lin, S., Genomic understanding of dinoflagellates, Res. Microbiol., 2011, vol. 162, pp. 551–569.

    Article  CAS  PubMed  Google Scholar 

  21. Moreno Diaz de la Espina, S., Alverca, E., Cuadrado, A., and Franca, S., Organization of the genome and gene expression in a nuclear environment lacking histones and nucleosomes: the amazing dinoflagellates, Eur. J. Cell. Biol., 2005, vol. 84, pp. 137–149.

    Article  CAS  PubMed  Google Scholar 

  22. Okamoto, O.K., Robertson, D.L., Fagan, T.F., Hastings, J.W., and Colepicolo, P., Different regulatory mechanisms modulate the expression of a dinoflagellate iron-superoxide dismutase, J. Biol. Chem., 2001, vol. 276, pp. 19989–19993.

    Article  CAS  PubMed  Google Scholar 

  23. Jones, G.D., Ernest, P., Williams, E.P., Place, A.R., Jagus, R., and Tsvetan, R., The alveolate translation initiation factor 4E family reveals a custom toolkit for translational control in core dinoflagellates, BMC Evol. Biol., 2015, vol. 15. e14

    Article  CAS  Google Scholar 

  24. Sigee, D.C., Structural DNA and genetically active DNA in dinoflagellate chromosomes, Biosyst., 1984, vol. 16, pp. 203–210.

    Article  CAS  Google Scholar 

  25. Soyer, M.O. and Haapala, O.K., Structural changes of dinoflagellate chromosome by pronase and ribonuclease, Chromosoma, 1974, vol. 47, vol. 179–192.

  26. Guillard, R.R.L. and Ryther, J.H., Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervaceae (Cleve) Gran, Can. J. Microbiol., 1962, vol. 8, pp. 229–239.

    Article  CAS  PubMed  Google Scholar 

  27. Kester, D.R., Duedall, I.W., Connors, D.N., and Pytkowicz, R.M., Preparation of artificial seawater, Limnol. Oceanogr., 1967, vol.12, pp. 176–179.

    Article  CAS  Google Scholar 

  28. Khlebovich, V.V., Acclimation of animal organisms: basic theory and applied aspects, Biol. Bull. Rev., 2017, vol. 7, no. 4, pp. 279–286.

    Article  Google Scholar 

  29. Rosic, N.N., Pernice, M., Dove, S., Dunn, S., and Hoegh-Guldberg, O., Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching, Cell Stress Chap., 2011, vol. 16, pp. 69–80.

    Article  CAS  Google Scholar 

  30. Schubert, H. and Telesh, I., Estuaries and coastal lagoons, Biological Oceanography of the Baltic Sea, Snoeijs-Leijonmalm, P., Schubert, H., and Radziejewska, T., Eds., Springer Science & Business Media Dordrecht, 2017, pp. 483–509.

  31. Schubert, H., Telesh, I., Nikinmaa, M., and Skarlato, S., Biological Oceanography of the Baltic Sea, Snoeijs-Leijonmalm, P., Schubert, H., and Radziejewska, T., Eds., Springer Science & Business Media Dordrecht, 2017, pp. 255–278.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. A. Knyazev.

Additional information

Original Russian Text © N.A. Knyazev, S.A. Pechkovskaya, S.O. Skarlato, I.V. Telesh, N.A. Filatova, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 5, pp. 339–345.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Knyazev, N.A., Pechkovskaya, S.A., Skarlato, S.O. et al. The Impact of Temperature Stress on DNA and RNA Synthesis in Potentially Toxic Dinoflagellates Prorocentrum minimum. J Evol Biochem Phys 54, 383–389 (2018). https://doi.org/10.1134/S002209301805006X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S002209301805006X

Key words

Navigation