Abstract
Although the water bodies of southern Russia experience the most extreme effects of cyanobacterial blooms, molecular genetic data on the composition of toxigenic cyanobacteria in this region have been absent. Screening for the genes responsible for the synthesis of hepatotoxins (microcystins and cylindrospermopsin) and neurotoxins (anatoxin-a and saxitoxins) in cyanobacteria from the Tsimlyansk Reservoir on the Don River was carried out. The presence of microcystin-producing Microcystis and Planktothrix populations, as well as of cyanobacteria capable of synthesis of a neurotoxin anatoxin-a, was revealed by polymerase chain reaction (PCR). A hypothesis of the presence of anatoxin-a-producing Planktothrix rubescens population in the phytoplankton of the Tsimlyansk Reservoir is proposed. The obtained PCR data were confirmed by the results of enzyme-linked immunosorbent assay (ELISA) and liquid chromatography/mass-spectrometry (LC/MS). Anatoxin-a and five microcystin variants were identified in the phytoplankton biomass.
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Apeldoorn, M.E., 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.
Ballot, A., Fastner, J., Lentz, M., and Wiedner, C., First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany, Toxicon, 2010a, vol. 56, pp. 964–971.
Ballot, A., Fastner, J., and Wiedner, C., Paralytic shellfish poisoning toxin-producing cyanobacterium Aphanizomenon gracile in Northeast Germany, Appl. Environ. Microbiol., 2010b, vol. 76, pp. 1173–1180.
Barón-Sola, Á, Ouahid, Y., and Campo, F., Detection of potentially producing cylindrospermopsin and microcystin strains in mixed populations of cyanobacteria by simultaneous amplification of cylindrospermopsin and microcystin gene regions, Ecotoxicol. Environ. Safety, 2012, vol. 75, pp. 102–108.
Edwards, C., Lawton, L.A., Beattie, K.A., Codd, G.A., Pleasance, S., and Dear, G.J., Analysis of microcystins from cyanobacteria by liquid chromatography with mass spectrometry using atmospheric pressure ionization, Rapid Commun. Mass Spectrom., 1993, vol. 7, no. 8, pp. 714–721.
Fastner, J., Erhard, M., Carmichael, W.W., Sun, F., Rinehart, K.L., and Chorus, I., Characterization and diversity of microcystin in natural blooms and strains of the genera of Microcystis and Planktothrix from German freshwaters, Arch. Hydrobiol., 1999, vol. 145, pp. 147–163.
Furey, A., Crowley, J., Hamilton, B., Lehane, M., and James, K.J., Strategies to avoid the mis-identification of anatoxin-a using mass spectrometry in the forensic investigation of acute neurotoxic poisoning, J. Chromatogr. A., 2005, vol. 1082, pp. 91–97.
Golokolenova, T.B., Development of Planktothrix agardhii (Gom.) Anagn. et Kom. in the Tsimlyansk Reservoir, Biologiya vnutrennikh vod (Biology of Inland Waters,) Proc. 13th Ith. School-Conf, Garin, E.V. et al., Eds., Rybinsk: Rybinskii Dom Pechati, 2007, pp. 57–63.
Gugger, M., Lenoir, S., Berger, C., Ledreux, A., Druart, J.C., Humbert, J.F., Guette, C., and Bernard, C., First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis, Toxicon, 2005, vol. 45. pp. 919–928.
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.
Komárek, J., Cyanoprokaryota 3. Teil. Heterocytous Genera, in Sußwasserflora von Mitteleuropa. Bd. 19 (3), Berlin: Springer, 2013.
Komárek, J. and Anagnostidis, K,. Cyanoprokaryota 1. Teil. Chroococcales, in Sußwasserflora von Mitteleuropa. Bd. 19 (1), Jena: Gustav Fischer, 1998.
Komárek, J. and Anagnostidis, K., Cyanoprokaryota 2. Teil. Oscillatoriales, in Sußwasserflora von Mitteleuropa. Bd. 19 (2), München: Elsevier, 2005.
Kuchishkina, N.V., Chemical composition of Tsimlyans Reservoir water at the present stage, in Rybokhozyaistvennye issledovaniya v basseine Volgo-Donskogo mezhdurech’ya na sovermennom etape (Fish Indusrty Research in the Volga–Don Interfluve Area at the Present Stage), Ivanov, D.I., Ed., SPb: GosNIORKh, 2002, pp. 16–28.
Kurmayer, R., Christiansen, G., Fastner, J., and Börner, T., Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobcterium Planktothrix spp., Environ. Microbiol., 2004, no. 6, pp. 831–841.
Kuz’min, G.V., Phytoplankton, species composition and abundance, in Metodika izucheniya biogeotsenozov vnutrennikh vodoemov (Methods for Investigation the Biogeocenoses of Inland Waters), Mordukhai-Boltovskii, F.D., Ed., Moscow: Nauka, 1975, pp. 73–87.
Lapitskii, I.I., Dierctional ichtiofauna formation and control of fish population abundance in Tsimlyansk Reservoir, Tr. Volgograd Otd. GosNIORKh, vol. 4, Volgograd: GOSNIORKh, 1970.
Lysak, T.B., Modern structural and functional characterization of the Tsimlyansk Reservoir summer phytoplankton, in Rybokhozyaistvennye issledovaniya v basseine Volgo-Donskogo mezhdurech’ya na sovermennom etape (Fish Indusrty Research in the Volga–Don Interfluve Area at the Present Stage), Ivanov, D.I., Ed., SPb: GosNIORKh, 2002, pp. 29–38.
Matishov, G.G. and Kovaleva, G.V., Water blooms in South Russian water bodies and water supply failures (exemplified by Volgodonsk City), Vestn. Yuzhn. Nauch. Tserntr RAN, 2010, vol. 6, no. 1, pp. 71–79.
Matishov, G.G., Matishov, D.G., Fushtei, T.V., Rudnev, M.I., Soier, V.G., and Zimakov, D.V., Detection of cyanoprokaryotic toxins in the Lower Don plankton by mass spectrometry, Vestn. Yuzhn. Nauch. Tserntr RAN, 2006, vol. 2, no. 2, pp. 75–78.
Mazur-Marzec, H., Spoof, L., Kobos, J., Plinski, M., and Meriluoto, J., Cyanobacterial hepatotoxins, microcystins and nodularins, in fresh and brackish waters of the Pomeranian Province, northern Poland, Oceanol. Hydrobiol. Studies, 2008, vol. 37, no. 4, pp. 3–21.
Meriluoto, J. and Spoof, L., Cyanotoxins: sampling, sample processing and toxin uptake, in Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs. Advances in Experimental Medicine and Biology, Kenneth, H.H., Ed., Berlin: Springer, 2008, vol. 619, pp. 483–499.
Methodical recommendations for collection and treatment of materials and hydrochemical investigation in freshwater basins, in Fitoplankton i ego produktsiya (Phytoplankton and Its Production), Vinberg, G.G., Ed., Leningrad: GosNIORKh, 1984.
Rantala, A., Rajaniemi-Wacklin, P., Lyra, C., Lepistö, L., Rintala, J., Mankiewicz-Boczek, J., and Sivonen, K., Detection of microcystin-producing cyanobacteria in Finnish lakes with genus-specific microcystin synthetase gene E (mcyE) PCR and associations with environmental factors, Appl. Environ. Microbiol., 2006, vol. 72, pp. 6101–6110.
Rantala-Ylinen, A., Känä, S., Wang, H., Rouhiainen, L., Wahlsten, M., Rizzi, E., Berg, K., Gugger, M., and Sivonen, K., Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. strain 37 and molecular methods to detect potential producers, Appl. Environ. Microbiol., 2011, vol. 77, pp. 7271–7278.
Sivonen, K. and Jones, G., Cyanobacterial toxins, in Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management, Chorus, I. and Bartram, J., Eds., London: E&FN Spon, 1999, pp. 41–111.
Spoof, L., Microcystins and nodularins, in Toxic: Cyanobacterial Monitoring and Cyanotoxins Analysis, Meriluoto, J. and Codd, G.A., Eds., Abo: Akademi University Press, 2005, pp. 15–39.
Spoof, L., Vesterkvist, P., Lindholm, T., and Meriluoto, J., Screening for hepatotoxins, microcystins and nodularin in environmental water samples by reversed-phase liquid chromatography-electrospray ionization mass spectrometry, J. Chromatogr. A., 2003, vol. 1020, pp. 105–119.
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.
Viaggiu, E., Melchiorre, S., Fabrizio, V., Di Corcia, A., Mancini, R., Garibaldi, L., Crichigno, G., and Bruno, M., Anatoxin-a in the cyanobacterium Planktothrix rubescens from a fishing pond in Northern Italy, Environ. Toxicol., 2004, vol.19, pp. 191–197.
Yuan, M., Namikoshi, M., Otsuki, A., Rinehart, K.L., Sivonen, K., and Watanabe, M.F., Low-energy collisionally activated decomposition and structural characterization of cyclic heptapeptide microcystins by electrospray ionization mass spectrometry, J. Mass Spectrom., 1999, vol. 34, no. 1, pp. 33–43.
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Original Russian Text © S.I. Sidelev, T.B. Golokolenova, E.N. Chernova, Ya.V. Russkikh, 2015, published in Mikrobiologiya, 2015, Vol. 84, No. 6, pp. 732–742.
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Sidelev, S.I., Golokolenova, T.B., Chernova, E.N. et al. Analysis of phytoplankton in Tsimlyansk Reservoir (Russia) for the presence of cyanobacterial hepato- and neurotoxins. Microbiology 84, 828–837 (2015). https://doi.org/10.1134/S0026261715060120
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DOI: https://doi.org/10.1134/S0026261715060120