Skip to main content
Log in

Limnological Characterization and First Data on the Occurrence of Toxigenic Cyanobacteria and Cyanotoxins in the Plankton of Some Lakes in the Permafrost Zone (Yakutia, Russia)

  • Published:
Contemporary Problems of Ecology Aims and scope

Abstract

The first data on the distribution of cyanobacterial toxins have been obtained and a molecular genetic determination of cyanotoxin producers in the plankton of some lakes in the permafrost zone in Yakutia have been performed for the first time. Most of the lakes are characterized by high concentrations of nitrogen, phosphorus, and chlorophyll a and by an increased content of organic matter, which could be associated with a high anthropogenic load. Water blooms were visually observed in three of the six studied lakes during the summer period. The abundance and biomass of cyanobacteria in the lakes varied within 13.7–676.3 million cells/L and 0.6–4.8 mg/L, respectively. Eight species of potentially toxigenic cyanobacteria were found in phytoplankton using light microscopy. Regions of the mcyE gene involved in the biosynthesis of microcystin were amplified using the polymerase chain reaction method in environmental DNA isolated from planktonic samples. Cyanobacteria capable of producing neurotoxic anatoxin-a, saxitoxins, and hepatotoxic nodularins were absent in the lakes during the study period. The use of genus-specific primers to the mcyE gene enables us to find that the main producers of microcystins were represented by species of the genus Microcystis in most of the lakes and by species of Dolichospermum only in one of the lakes. Up to eight structural variants of microcystins, in general, arginine-containing isoforms MC-LR, MC-RR, MC-YR, MC-LY, MC-HIlR, [Asp3]MC-LR, [Asp3]MC-RR, and [Asp3]MC-YR, were identified in lake plankton using liquid chromatography–mass spectrometry. The maximal concentration of microcystins in plankton (intracellular fraction 803 ng/L) was recorded in a sample from Ytyk-Kyuyol Lake. The calculated content of microcystins per unit biomass of producing cyanobacteria (toxin quota) was low (0.005–0.069 µg/mg). In order to assess the potential hazard of toxigenic species of cyanobacteria to human health, the distribution of cyanotoxins and their producers should be further studied in water bodies of the region.

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.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Arzhakova, S.K., Zhirkov, I.I., Kusatov, K.I., and Androsov, I.M., Reki i ozera Yakutii: kratkii spravochnik (Rivers and Lakes of Yakutia: a Brief Guide), Yakutsk: Bichik, 2007.

  2. Ballot, A., Fastner, J., and Wiedner, C., Paralytic shellfish poisoning toxin-producing cyanobacterium Aphanizomenon gracile in Northeast Germany, Appl. Environ. Microbiol., 2010, vol. 76, pp. 1173–1180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bernard, C., Ballot, A., Thomazeau, S., Maloufi, S., Furey, A., Mankiewicz-Boczek, J., Pawlik-Skowrońska, B., Capelli, C., and Salmaso, N., Cyanobacteria associated with the production of cyanotoxins, in Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis, Meriluoto, J., Spoof, L., and Codd, G.A., Eds., Chichester, West Sussex: John Wiley & Sons, 2017, pp. 501–525.

    Google Scholar 

  4. Bober, B. and Bialczyk, J., Determination of the toxicity of the freshwater cyanobacterium Woronichinia naegeliana (Unger) Elenkin, J. Appl. Phycol., 2017, vol. 29, pp. 1355–1362.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Botana, L., Seafood and Freshwater Toxins. Pharmacology, Physiology and Detection, Boca Raton: CRC, 2008.

    Google Scholar 

  6. Casero, M.C., Ballot, A., Agha, R., Quesada, A., and Cires, S., Characterization of saxitoxin production and release and phylogeny of sxt genes in paralytic shellfish poisoning toxin-producing Aphanizomenon gracile, Harmful Algae, 2014, vol. 37, pp. 28–37.

    Article  CAS  Google Scholar 

  7. Chernova, E., Russkikh, I., Voyakina, E., and Zhakovskaya, Z., Occurrence of microcystins and anatoxin-a in eutrophic lakes of Saint Petersburg, Northwestern Russia, Oceanol. Hydrobiol. Stud., 2016, vol. 45, no. 4, pp. 466–484.

    Article  CAS  Google Scholar 

  8. Chernova, E.N., Russkikh, Ya.V., Podolskaya, E.P., and Zhakovskaya, Z.A., Determination of microcystins and anatoxin-a using liquid chromato-mass-spectrometry of unit resolution, Nauchn. Priborostr., 2016, vol. 26, no. 1, pp. 11–25.

    Article  Google Scholar 

  9. Chernova, E., Sidelev, S., Russkikh, I., Korneva, L., Solovyova, V., Mineeva, N., Stepanova, I., and Zhakovskaya, Z., Spatial distribution of cyanotoxins and ratios of microcystin to biomass indicators in the reservoirs of the Volga, Kama and Don Rivers, the European part of Russia, Limnologica, 2020, vol. 84, p. 125819.

    Article  CAS  Google Scholar 

  10. Chorus, I. and Welker, M., Toxic Cyanobacteria in Water, Boca Raton: CRC, 2021.

    Book  Google Scholar 

  11. Chrapusta, E., Wegrzyn, M., Zabaglo, K., Kaminski, A., Adamski, M., Wietrzyk, P., and Bialczyk, J., Microcystins and anatoxin-a in Arctic biocrust cyanobacterial communities, Toxicon, 2015, vol. 101, pp. 35–40.

    Article  CAS  PubMed  Google Scholar 

  12. Cires, S. and Ballot, A., A review of the phylogeny, ecology and toxin production of bloom-forming Aphanizomenon spp. and related species within the Nostocales (cyanobacteria), Harmful Algae, 2016, vol. 54, pp. 21–43.

    Article  CAS  PubMed  Google Scholar 

  13. Cires, S., Casero, M., and Quesada, A., Toxicity at the edge of life: a review on cyanobacterial toxins from extreme environments, Mar. Drugs, 2017, vol. 15, no. 7, pp. 1–18.

    Article  Google Scholar 

  14. Denisov, D.B. and Kashulin, N.A., Cyanoprokaryotes in the composition of the plankton of Imandra Lake (Kola Peninsula), Tr. Kol’sk. Nauchn. Tsentra Ross. Akad. Nauk, 2016, vol. 4, no. 7(41), pp. 40–57.

  15. Denisov, D.B., Chernova, E.N., and Russkikh, I.V., Toxic Cyanobacteria in the Arctic Lakes: New environmental challenges. A case study, in Advanced Technologies for Sustainable Development of Urban Green Infrastructure, Vasenev, V., Eds., Berlin: Springer-Verlag, 2021, pp. 161–170.

    Google Scholar 

  16. Fastner, J., Wirsing, B., Wiedner, C., Heinze, R., Neumann, U., and Chorus, I., Microcystins and hepatocyte toxicity, in Cyanotoxins: Occurrence, Causes, Consequences, Chorus, I., Ed., Berlin: Springer-Verlag, 2001, pp. 22–37.

    Google Scholar 

  17. Field, C.B., Barros, V.R., Dokken, D.J., Mach, K.J., Mastrandrea, M.D., Bilir, T.E., Chatterjee, M., Ebi, K.L., Estrada, Y.O., Genova, R.C., Girma, B., Kissel, E.S., Levy, A.N., MacCracken, S., Mastrandrea, P.R., and White, L.L., IPCC 2014: Summary for policymakers in Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects, in Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge: Cambridge Univ., 2014, pp. 1–32.

    Google Scholar 

  18. Fontes, A.G., Angeles Vargas, M., Moreno, J., Guerrero, M.G., and Losada, M., Factors affecting the production of biomass by a nitrogen-fixing blue-green alga in outdoor culture, Biomass, 1987, vol. 13, pp. 33–43.

    Article  CAS  Google Scholar 

  19. Furey, A., Allis, O., Ortea, P.M., Lehane, M., and James, K.J., Hepatotoxins: context and chemical determination, in Seafood and Freshwater Toxins. Pharmacology, Physiology and Detection, Botana, L., Ed., Boca Raton: CRC Press, Taylor & Francis Group, 2008, pp. 844–886.

    Google Scholar 

  20. Hitzfeld, B.C., Lampert, C.S., Spaeth, N., Mountfort, D., Kaspar, H., and Dietrich, D.R., Toxin production in cyanobacterial mats from ponds on the McMurdo Ice Shelf, Antarctica, Toxicon, 2000, vol. 38, pp. 1731–1748.

    Article  CAS  PubMed  Google Scholar 

  21. Huisman, J., Codd, G.A., Paerl, H.W., Ibelings, B.W., Verspagen, J.M.H., and Visser, P.M., Cyanobacterial blooms, Nat. Rev. Microbiol., 2018, vol. 16, pp. 471–483.

    Article  CAS  PubMed  Google Scholar 

  22. Humpage, A., Toxin types, toxicokinetics and toxicodynamics, in Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs, Hudnell, H.K., Ed., New York: Springer-Verlag, 2008.

    Google Scholar 

  23. Ivanova, A.P., Algae of urban and suburban lakes of the Middle Lena Valley, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Yakutsk, 2000.

  24. Jakubowska, N. and Szeląg-Wasielewska, E., Toxic picoplanktonic cyanobacteria—Review, Mar. Drugs, 2015, vol. 13, no. 3, pp. 1497–1518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Jungblut, A.D. and Neilan, B.A., Molecular identification and evolution of the cyclic peptide hepatotoxins, microcystin and nodularin, synthetase genes in three orders of cyanobacteria, Arch. Microbiol., 2006, vol. 185, pp. 107–114.

    Article  CAS  PubMed  Google Scholar 

  26. Jungblut, A.D., Hoeger, S.J., Mountfort, D., Hitzfeld, B.C., Dietrich, D.R., and Neilan, B.A., Characterization of microcystin production in an Antarctic cyanobacterial mat community, Toxicon, 2006, vol. 47, pp. 271–278.

    Article  CAS  PubMed  Google Scholar 

  27. Kleinteich, J., Wood, S., Küpper, F., Camacho, A., Quesada, A., Frickey, T., and Dietrich, D., Temperature-related changes in polar cyanobacterial mat diversity and toxin production, Nat. Clim. Change, 2012, vol. 2, pp. 356–360.

    Article  CAS  Google Scholar 

  28. Kleinteich, J., Wood, S.A., Puddick, J., Schleheck, D., Küpper, F.C., and Dietrich, D., Potent toxins in Arctic environments – Presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems, Chem. Biol. Interact., 2013, vol. 206, no. 2, pp. 423–431.

    Article  CAS  PubMed  Google Scholar 

  29. Kleinteich, J., Hildebrand, F., Wood, S., Cirés, S., Agha, R., Quesada, A., Pearce, D.A., Convey, P., Küpper, F.C., and Dietrich, D.R., Diversity of toxin and non-toxin containing cyanobacterial mats of meltwater ponds on the Antarctic Peninsula: A pyrosequencing approach, Antarct. Sci., 2014, vol. 26, pp. 521–532.

    Article  Google Scholar 

  30. Komárek, J. and Anagnostidis, K., Cyanoprokaryota, vol. 1: Chroococcales, Jena: Gustav Fischer Verlag, 1998.

    Google Scholar 

  31. Komárek, J. and Anagnostidis, K., Cyanoprokaryota, vol. 2: Oscillatoriales, München: Elsevier, 2005.

    Google Scholar 

  32. Komárek, J. and Anagnostidis, K., Cyanoprokaryota, vol. 3: Heterocytous genera, Berlin: Springer-Verlag, 2013.

    Google Scholar 

  33. Lyon-Colbert, A., Su, S., and Cude, C., A systematic literature review for evidence of Aphanizomenon flos-aquae toxigenicity in recreational waters and toxicity of dietary supplements: 2000-2017, Toxins, 2018, vol. 10, no. 7, p. 254.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Magnuson, J.J., Robertson, D.M., Benson, B.J., Wynne, R.H., Livingstone, D.M., Arai, R.A., Barry, R.G., Card, V., Kuusisto, E., Granin, N.G., Prowse, T.D., Stewart, K.M., and Vuglinski, V.S., Historical trends in lake and river ice cover in the Northern Hemisphere, Science, 2000, vol. 289, no. 5485, pp. 1743–1746.

    Article  CAS  PubMed  Google Scholar 

  35. Makarova, I.V. and Pichkily, L.O., On some issues of the plankton biomass calculation method, Bot. Zh., 1970, vol. 55, no. 10, pp. 1448–1494.

    Google Scholar 

  36. Mariani, M., Padedda, B., Kaštovský, J., Buscarinu, P., Sechi, N., Virdis, T., and Lugliè, A., Effects of trophic status on microcystin production and the dominance of cyanobacteria in the phytoplankton assemblage of Mediterranean reservoirs, Sci. Rep., 2015, vol. 5, p. 17964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Meriluoto, J., Spoof, L., and Codd, G.A., Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis, Chichester, West Sussex: John Wiley & Sons, 2017.

    Google Scholar 

  38. Nürnberg, G.K. and Peters, R.H., Biological availability of soluble reactive phosphorus in anoxic and oxic freshwaters, Can. J. Fish. Aquat. Sci., 1984, vol. 41, no. 5, pp. 757–765.

    Article  Google Scholar 

  39. Nürnberg, G.K., Trophic state of clear and colored, soft- and hardwater lakes with special consideration of nutrients, anoxia, phytoplankton an fish, J. Lake Reservoir Manage., 1996, vol. 12, pp. 432–447.

    Article  Google Scholar 

  40. Paerl, H.W. and Paul, V.J., Climate change: Links to global expansion of harmful cyanobacteria, Water Res., 2012, vol. 46, pp. 1349–1363.

    Article  CAS  PubMed  Google Scholar 

  41. Resursy poverkhnostnykh vod SSSR. T. 1. Kol’skii poluostrov. (Resources of Surface Waters of the USSR. T. 1. Kola Peninsula), Leningrad: Gidrometeoizdat, 1970.

  42. Rinehart, K.L., Namikoshi, M., and Choi, B.W., Structure and biosynthesis of toxins from blue-green algae (cyanobacteria), J. Appl. Phycol., 1994, vol. 6, pp. 159–176.

    Article  CAS  Google Scholar 

  43. Rinehart, K.L., Namikoshi, M., and Choi, B.W., Structure and biosynthesis of toxins from blue-green algae (cyanobacteria), J. Appl. Phycol., 1994, vol. 6, pp. 159–176.

    Article  CAS  Google Scholar 

  44. Rukovodstvo po metodam gidrobiologicheskogo analiza poverhnostnykh vod i donnykh otlozhenii (Guidelines on Methods for Hydrobiological Analysis of Surface Waters and Bottom Sediments), Abakumov, V.A., Leningrad: Gidrometeoizdat, 1983.

  45. Safonova, T.A. and Ermolaev, V I., Vodorosli vodoemov sistemy ozera Chany (Algae of Water Bodies of the Chany Lake System), Novosibirsk: Nauka, 1983.

  46. Samarina, V.S., Gidrogeokhimiya (Hydrogeochemistry), Leningrad: Leningr. Gos. Univ., 1977.

    Google Scholar 

  47. Semenov, A.D., Rukovodstvo po khimicheskomu analizu poverkhnostnykh vod sushi (Guidance on the Chemical Analysis of Surface Inner Waters), Leningrad, 1977.

    Google Scholar 

  48. Sidelev, S., Zubishina, A., and Chernova, E., Distribution of microcystin-producing genes in Microcystis colonies from some Russian freshwaters: Is there any correlation with morphospecies and colony size?, Toxicon, 2020, vol. 184, pp. 136–142.

    Article  CAS  PubMed  Google Scholar 

  49. Sivonen, K. and Jones, G., Cyanobacterial toxins, in Toxic Cyanobaceria in Water: a Guide to their Public Health Consequences, Monitoring and Management, Chorus, I. and Bartram, J., Eds., London: E & FN Spon, 1999.

    Google Scholar 

  50. Smirnova, V.S., Tekanova, E.V., Kalinkina, N.M., and Chernova, E.N., Status of phytoplankton and cyanotoxins in the “bloom” spot in Svyatozero Lake (Lake Onega basin, Russia), Voda Ekol.: Probl. Resheniya, 2021, vol. 1, no. 85, pp. 50–60.

    Google Scholar 

  51. Svirčev, Z., Lalić, D., Savić, B.G., Tokodi, N., Drobac, B.D., Chen, L., Meriluoto, J., and Codd, G.A., Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings, Arch. Toxicol., 2019, vol. 93, pp. 2429–2481.

    Article  PubMed  Google Scholar 

  52. Tonk, L., Bosch, K., Visser, P.M., and Huisman, J., Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa, Aquat. Microb. Ecol., 2007, vol. 46, pp. 117–123.

    Article  Google Scholar 

  53. Trout-Haney, J.V., Wood, Z.T., and Cottingham, K.L., Presence of the cyanotoxin microcystin in arctic lakes of southwestern Greenland, Toxins, 2016, vol. 8, no. 9, p. 256.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Trout-Haney, J., Ritger, A., and Cottingham, K., Benthic cyanobacteria of the genus Nostoc are a source of microcystins in Greenlandic lakes and ponds, Freshwater Biol., 2021, vol. 66, pp. 266–277.

    Article  CAS  Google Scholar 

  55. Vaitomaa, J., Rantala, A., Halinen, K., Rouhiainen, L., Tallberg, P., Mokelke, L., and Sivonen, K., Quantitative real-time PCR for determination of microcystin synthetase gene E copy numbers for Microcystis and Anabaena in lakes, Appl. Environ. Microbiol., 2003, vol. 69, pp. 7289–7297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. van Apeldoorn, M.E., van Egmond, H.P., Speijers, G.J.A., and Bakker, G.J.I., Toxins of cyanobacteria, Mol. Nutr. Food Res., 2007, vol. 51, pp. 7–60.

    Article  CAS  PubMed  Google Scholar 

  57. Vasilieva I. I. Composition and seasonal dynamics of phytoplankton in lakes around the city of Yakutsk, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Novosibirsk, 1968.

  58. Voloshko, L., Kopecky, J., Safronova, T., Pljusch, A., Titova, N., Hrouzek, P., and Drabkova, V., Toxins and other bioactive compounds produced by cyanobacteria in Lake Ladoga, Est. J. Ecol., 2008, vol. 57, pp. 100–110.

    Google Scholar 

  59. Vuglinsky, V. and Valatin, D., Changes in ice cover duration and maximum ice thickness for rivers and lakes in the Asian part of Russia, Nat. Resour., 2018, vol. 9, pp. 73–87.

    Google Scholar 

  60. Wang, X., Hao, C., Zhang, F., Feng, C., and Yang, Y., Inhibition of the growth of two blue-green algae species (Microsystis aruginosa and Anabaena spiroides) by acidification treatments using carbon dioxide, Bioresour. Technol., 2011, vol. 102, pp. 5742–5748.

    Article  CAS  PubMed  Google Scholar 

  61. Wetzel, R.G., Limnology: Lake and River Ecosystems, San Diego: Academic, 2001.

    Google Scholar 

  62. Willame, R., Jurczak, T., Kull, T., Meriluoto, J., and Homann, L., Distribution of hepatotoxic cyanobacterial blooms in Belgium and Luxembourg, Hydrobiologia, 2005, vol. 551, pp. 99–117.

    Article  CAS  Google Scholar 

  63. Winder, M. and Sommer, U., Phytoplankton response to a changing climate, Hydrobiologia, 2012, vol. 698, pp. 5–16.

    Article  Google Scholar 

  64. Wood, S.A., Mountfort, D., Selwood, A.I., Holland, P.T., Puddick, J., and Cary, S.C., Widespread distribution and identification of eight novel microcystins in Antarctic cyanobacterial mats, Appl. Environ. Microbiol., 2008, vol. 74, pp. 7243–7251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was performed as part of state task of the Ministry of Science and Education of the Russian Federation no. FWRS-2021-0023, EGISU NIOKTR no. АААА-А21-121012190038-0, and within the framework of state budgetary theme no. FFZF-2022-0012, RosRid no. 122041100086-5. Molecular genetic studies were performed by S.I. Sidelev at the Scientific and Educational Laboratory of Molecular Genetics and Biotechnology, Yaroslavl State University, as part of the Yaroslavl State University Development Program (NIR no. P2-GL3-2022).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to V. A. Gabyshev, S. I. Sidelev or E. N. Chernova.

Ethics declarations

The authors declare that they have no conflicts of interest.

Additional information

Translated by I. Bel’chenko

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gabyshev, V.A., Sidelev, S.I., Chernova, E.N. et al. Limnological Characterization and First Data on the Occurrence of Toxigenic Cyanobacteria and Cyanotoxins in the Plankton of Some Lakes in the Permafrost Zone (Yakutia, Russia). Contemp. Probl. Ecol. 16, 89–102 (2023). https://doi.org/10.1134/S1995425523020087

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1995425523020087

Keywords:

Navigation