On the occurrence and toxicity of Cylindrospermopsis raciborskii in Poland

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Abstract

Cylindrospermopsis raciborskii which belongs to the order of Nostocales has continuously been at the centre of interest of various research groups owing to its great ecological plasticity, wide distribution and potential to produce different metabolites known to be harmful for humans and animals. Over recent decades, Polish strains of C. raciborskii have also been studied with regard to these issues. The present paper is a brief review of the present state of knowledge respecting the occurrence and toxicity of this species with emphasis on Polish strains, and indicates potential directions for future research.

Acs A., Kovács A.W., Csepregi J.Z., Törő N., Kiss G., Győri J., Vehovszky A., Kováts N., Farkas A., 2013, The ecotoxicological evaluation of Cylindrospermopsis raciborskii from Lake Balaton (Hungary) employing a battery of bioassays and chemical screening, Toxicon 70: 98–106.

Antal O., Karisztl-Gácsi M., Farkas A., Kovács A., Acs A., Töro N., Kiss G., Saker M.L., Gyori J., Bánfalvi G., Vehovszky A., 2011, Screening the toxic potential of Cylindrospermopsis raciborskii strains isolated from Lake Balaton, Hungary, Toxicon 57: 831–840.

Antunes J.T., Leão P.N., Vasconcelos V.M., 2015, Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species, Front. Microbiol. 6: 473.

Babanazarova O.V., Sidelev S.I., Fastner J., 2015, Northern expansion of Cylindrospermopsis raciborskii (Nostocales, Cyanoprokaryota) observed in shallow highly eutrophic lake Nero (Russia), Int. J. Algae 17(2): 131–141.

Ballot A., Fastner J., Wiedner C., 2010, Paralytic shellfish poisoning toxin-producing cyanobacterium Aphanizomenon gracile in Northeast Germany, Appl. Environ. Microb. 76(4): 1173–1180.

Bernard C., Harvey M., Briand J.F., Biré R., Krys S., Fontaine J.J., 2003, Toxicological comparison of diverse Cylindrospermopsis raciborskii strains: evidence of liver damage caused by a French C raciborskii strain, Environ. Toxicol. 18(3): 176–186.

Bonilla S., Aubriot L., Soares M.C., González-Piana M., Fabre A., Huszar V.L., Lürling M., Antoniades D., Padisák J., Kruk C.., 2012, What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii?, FEMS Microbiol. Ecol. 79(3): 594–607.

Bonilla S., Gonzáles-Piana M., Soares M. C. S., Huszar V. L. M., Becker V., Somma A., Marinho M. M., Kokociński M., Dokulil M., Antoniades D., Abriot L., 2016, The success of the cyanobacterium Cylindrospermopsis raciborskii in freshwaters is enhanced by the combined effects of light intensity and temperature, J. Limnol. 75(3): 606–617.

Brygider A., Kokociński M., 2016, Cylindrospermopsis raciborskii – a growing ability of tropical cyanobacterium to adapt to conditions in temperate lakes of Western Poland (northern Greater Poland, lake Pniewskie and Kierskie Małe) [Abstract], Abstract book of the 11th International Conference of Young Naturalists “From Biotechnology to Environmental Protection” – Interdisciplinary Meeting of Young Naturalists, Zielona Góra, Poland, 23–26 November.

Bukowska A., Bielczyńska A., Karnkowska A., Chróst R.J., Jasser I., 2014, Molecular (PCR-DGGE) versus morphological approach: analysis of taxonomic composition of potentially toxic cyanobacteria in freshwater lakes, Aquat. Biosyst. 10: 2.

Burchardt L., Hindák F., Komárek J., Lange-Bertalot H., Messyasz B., Pikosz M., Wejnerowski Ł., Jakubas E., Rybak A., Gąbka M., 2014, Spring phytoplankton and periphyton composition: case study from a thermally abnormal lakes in Western Poland, Biodiv. Res. Conserv. 36: 17–24.

Burchardt L., 1977, Changes in phytoplankton composition of Lake Pątnowskie, receiver of heated waste water from sugar factory (1972/73), Ser. Biologia 8: 1–119.

Burford M.A., Beardall J., Willis A., Orr P.Y., Magalhaes V.F., Rangel L.M., Azevedo S.M.F.O.E., Neilan B.A., 2016, Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii, Harmful Algae 54: 44–53.

Chiswell R.K., Shaw G.R., Eaglesham G., Smith M.J., Norris R.L., Seawright A.A., Moore M.R., 1999, Stability of cylindrospermopsin the toxin from the cyanobacterium Cylindrospermopsis raciborskii: effect of pH temperature and sunlight on decomposition, Environ. Toxicol. 14(1): 155–161.

Chonudomkul D., Yongmanitchai W., Theeragool G., Kawachi M., Kasai F., Kaya K., Watanabe M.M., 2004, Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan, FEMS Microbiol. Ecol. 48(3): 345–355.

Cirés S., Wörmer L., Ballot A., Agha R., Wiedner C., Velázquez D., Casero M.C., Quesada A., 2014, Phylogeography of cylindrospermopsin and paralytic shellfish toxin-producing nostocales cyanobacteria from mediterranean europe (Spain), Appl. Environ. Microbiol. 80(4): 1359–7130.

Dorđević N., Simić S.B., Ciric A.R., 2015, First identification of the cylindrospermopsin (CYN) producting by cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju in Serbia, Fresenius Environ. Bull. 24(11a): 3736–3742.

Engström-Öst J., Rasic I.S., Brutemark A., Rancken R., Simić G.S., Laugen A.T., 2015, Can Cylindrospermopsis raciborskii invade the Baltic Sea?, Environ. Rev. 23(2): 161–169.

Fathalli A., Jenhani A.B., Moreira C., Azevedo J., Welker M., Romdhane M., Antunes A., Vasconcelos V., 2011, Genetic variability of the invasive cyanobacteria Cylindrospermopsis raciborskii from Bir M'cherga reservoir (Tunisia), Arch. Microbiol. 193(8): 595–604.

Fastner J., Heinze R., Humpage A.R., Mischke U., Eaglesham G.K., Chorus I., 2003, Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates, Toxicon 42: 313–321.

Gkelis S., Zaoutsos N., 2014, Cyanotoxin occurrence and potentially toxin producing cyanobacteria in freshwaters of Greece: a multi-disciplinary approach, Toxicon 78: 1–9.

Gugger M., Molica R., Le Berre B., Dufour P., Bernard C., Humbert J.-F., 2005, Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) isolated from four continents, Appl. Environ. Microbiol. 71(2): 1097–1100.

Hawkins P.R., Chandrasena N.R., Jones G.J., Humpage A.R., Falconer I.R., 1997, Isolation and toxicity of Cylindrospermopsis raciborskii from an ornamental lake, Toxicon 35: 341–346.

Hoff-Risseti C., Dorr F.A., Schaker P.D.C., Pinto E., Werner V.R., Fiore M.F., 2013, Cylindrospermopsin and saxitoxin synthetase genes in Cylindrospermopsis raciborskii strains from Brazilian freshwater, PLoS ONE 8(8): e74238.

Holland A., Kinnear S., 2013. Interpreting the possible ecological role(s) of cyanotoxins: compounds for competitive advantage and/or physiological aide?, Mar. Drugs 11(7): 2239–2258.

Jaja-Chimedza A., Gantar M., Gibbs P.D., Schmale M.C., Berry J.P., 2012, Polymethoxy-1-alkenes from Aphanizomenon ovalisporum inhibit vertebrate development in the zebrafish (Danio rerio) embryo model, Mar. Drugs 10(10): 2322–2336.

Jaja-Chimedza A., Saez C., Sanchez K., Gantar M., Berry J.P., 2015, Identification of teratogenic polymethoxy-1-alkenes from Cylindrospermopsis raciborskii, and taxonomically diverse freshwater cyanobacteria and green algae, Harmful Algae 49: 156–161.

Jakubowska N., Zagajewski P., Gołdyn R., 2013, Water blooms and cyanobacterial toxins in lakes, Pol. J. Environ. Stud. 22(4): 1077–1082.

Karadžić V., Simić G.S., Natić D., Ržaničanin A., Ćirić M., Gačić Z., 2013, Changes in the phytoplankton community and dominance of Cylindrospermopsis raciborskii (Wolosz.) Subba Raju in a temperate lowland river (Ponjavica, Serbia), Hydrobiologia 711: 43–60.

Kobos J., Błaszczyk A., Hohlfeld N., Toruńska-Sitarz A., Krakowiak A., Hebel A., Sutryk K., Grabowska M., Toporowska M., Kokociński M., Messyasz B., Rybak A., Napiórkowska-Krzebietke A., Nawrocka L., Pełechata A., Budzyńska A., Zagajewski P., Mazur-Marzec H., 2013, Cyanobacteria and cyanotoxins in Polish freshwater bodies, Oceanol. Hydrobiol. Stud. 42(4): 358–378.

Kokociński M., Stefaniak K., Mankiewicz-Boczek J., Izydorczyk K., Soininen J., 2010, The ecology of the invasive cyanobacterium Cylindrospermopsis raciborskiii (Nostocales, Cyanophyta) in two hypereutrophic lakes dominated by Planktothrix agardhii (Oscillatoriales, Cyanophyta), Eur. J. Phycol. 45(4): 365–374.

Kokocinski M., Soininen J., 2012, Environmental factors related to the occurrence of Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) at the north-eastern limit of its geographical range, Eur. J. Phycol. 47(1): 12–21.

Kokociński M., Mankiewicz-Boczek J., Jurczak T., Spoof L., Meriluoto J., Rejmonczyk E., Hautala H., Vehniäinen M., Pawełczyk J., Soininen J., 2013, Aphanizomenon gracile (Nostocales), a cylindrospermopsin-producing cyanobacterium in Polish lakes, Environ. Sci. Pollut. Res. Int. 20(8): 5243–5264.

Kokociński M., Gągała I., Jassser I., Kobos J., Koreiviene J., Soininen J., Szczurowska A., Dziga D., Mankiewicz-Boczek J., 2016, Which environmental factors drive the distribution of potentially toxic Cylindrospermopsis raciborskii in Central-Eastern Europe? [Abstract], Abstract book of the 10th International Conference on Toxic Cyanobacteria, 23–28 October 2016, Wuhan (China): 26.

Lei L., Peng L., Huang X., Han B.P., 2014, Occurrence and dominance of Cylindrospermopsis raciborskii and dissolved cylindrospermopsin in urban reservoirs used for drinking water supply, South China, Environ. Monit. Assess. 186(5): 3079–3090.

Mankiewicz-Boczek J, Kokociński M, Gagała I, Pawełczyk J, Jurczak T, Dziadek J., 2012, Preliminary molecular identification of cylindrospermopsin-producing Cyanobacteria in two Polish lakes (Central Europe), FEMS Microbiol. Lett. 326(2): 173–179.

Mazmouz R., Chapuis-Hugon F., Mann S., Pichon V., Mejean A., Ploux O., 2010, Biosynthesis of cylindrospermopsin and 7-epicylindrospermopsin in Oscillatoria sp. strain PCC 6506: identification of the cyr gene cluster and toxin analysis, Appl. Environ. Microbiol. 76(15): 4943–4949.

Napiórkowska-Krzebietke A., 2009, Diversity and dynamics of phytoplankton in Lake Licheńskie and Lake Ślesińskie in 2004-2005, Arch. Pol. Fish. 17(4): 253–265.

Ohtani I., Moore R.E., Runnegar M.T.C., 1992, Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii, J. Am. Chem. Soc. 114(20): 7941–7942.

O'Neill K., Musgrave I.F., Humpage A., 2016, Low dose extended exposure to saxitoxin and its potential neurodevelopmental effects: A review, Environ. Toxicol. Pharmacol. 48: 7–16.

Panou M., Zervou S., Christophoridis C., Manolidi K., Triantis T., Kaloudis T., Hiskia A., Gkelis S., 2016, First report of a microcystin-producing Cylindrospermopsis raciborskii strain isolated from Greece [Abstract], Abstract book of the 10th International Conference on Toxic Cyanobacteria, 23–28 October 2016, Wuhan (China): 57.

Padisák J., Reynolds C.S., 1998, Selection of phytoplankton associations in Lake Balaton, Hungary, in response to eutrophication and restoration measures, with special reference to the cyanoprokaryotes, Hydrobiologia 384: 41–53.

Pełechata A., Ławniczak A.E., 2013, New localities of Cylindrospermopsis raciborskii and Anabaenopsis elenkinii within the Wielkopolska National Park, Western Poland [Abstract], Abstract book of the 32nd International Conference of Polish Phycologists “Do thermophilic species invasion threaten us?”, 20-23 May, Konin-Mikorzyn (Poland): 116–117.

Pełechata A., Pełechaty M., Pukacz A., 2006, Cyanoprokaryota of shallow lakes of Lubuskie Lakeland (mid-western Poland), Oceanol. Hydrobiol. Stud. 35(1): 3–14.

Poniedziałek B., Rzymski P., Kokociński M., 2012, Cylindrospermopsin: water-linked potential threat to human health in Europe, Environ. Toxicol. Pharmacol. 34(3): 651–660.

Poniedziałek B., Rzymski P., Kokociński M., Karczewski J., 2015, Toxic potencies of metabolite(s) of non-cylindrospermopsin producing Cylindrospermopsis raciborskii isolated from temperate zone in human white cells, Chemosphere 120: 608–614.

Preußel K., Wessel G., Fastner J., Chorus I., 2009, Response of cylindrospermopsin production and release in Aphanizomenon flos-aquae (Cyanobacteria) to varying light and temperature conditions, Harmful Algae 8(5): 645–650.

Rzymski P., Poniedziałek B., 2014, In search of environmental role of cylindrospermopsin: a review on global distribution and ecology of its producers, Water Res. 66: 320–327.

Rzymski P., Poniedziałek B., Kokociński M., Jurczak T., Lipski D., Wiktorowicz K., 2014, Interspecific allelopathy in cyanobacteria: cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa, Harmful Algae 35: 1–8.

Rzymski P., Poniedziałek B., Mankiewicz-Boczek J., Faassen E.J., Jurczak T., Gągała-Borowska I., Ballot A., Lürling M., Kokociński M., 2017, Polyphasic toxicological screening of Cylindrospermopsis raciborskii and Aphanizomenon gracile isolated in Poland, Algal Res. 24: 72–80.

Saker M.L., Nogueira I.C., Vasconcelos V.M., Neilan B.A., Eaglesham G.K., Pereira P., 2003, First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters, Ecotoxicol. Environ. Saf. 55(2): 243–250.

Sinha R, Pearson LA, Davis TW, Burford MA, Orr PT, Neilan BA., 2012, Increased incidence of Cylindrospermopsis raciborskii in temperate zones--is climate change responsible?, Water Res. 46(5): 1408–1419.

Skuja H., 1937, Süßwasseralgen aus Griechenland und Kleinasien, Hedwigia 77: 15–73.

Smutná M., Priebojová J., Večerková J., Hilscherová K., 2016, Retinoid-like compounds produced by phytoplankton affect embryonic development of Xenopus laevis, Ecotoxicol. Environ. Saf. 138: 32–38.

Soares M.C.S., Huszar V.L.M., Miranda M.N., Mello M.M., Roland F., Lürling M., 2013, Cyanobacterial dominance in Brazil: distribution and environmental preferences, Hydrobiologia 717: 1–12.

Stefaniak K. Kokociński M., 2005, Occurrence of invasive cyanobacteria species in polimictic lakes of the Wielkopolska region (Western Poland), Oceanol. Hydrobiol. Stud.34 (Suppl. 3): 137–148.

Svirčev Z., Obradović V., Codd G.A., Marjanović P., Spoof L., Drobac D., Tokodi N., Petković A., Nenin T., Simeunović J., Važić T., Meriluoto J., 2016, Massive fish mortality and Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake, Ecotoxicology 25(7): 1353–1363.

Vehovszky Á., Kovács A.W., Farkas A., Győri J., Szabó H., Vasas G., 2015, Pharmacological studies confirm neurotoxic metabolite(s) produced by the bloom-forming Cylindrospermopsis raciborskii in Hungary, Environ. Toxicol. 30(5): 501–512.

Waters M.N., 2016, A 4700-year history of cyanobacteria toxin production in a shallow subtropical lake, Ecosystems 19(3): 426–436.

Wiese M., D’Agostino P.M., Mihali T.K., Moffitt M., Neilan B.A., 2010, Neurotoxic alkaloids: Saxitoxin and its analogs, Mar. Drugs 8(7): 2185–2211.

Woloszynska J., 1912, Das Phytoplankton einiger Javanian Seen mit Berücksichtigung des Sawa-Planktons, Bull. Int. Acad. Sci. Cracoviae Ser. B 6: 649–709.

Wood S.A., Stirling D.J., 2003, First identification of the cylindrospermopsin-producing cyanobacterium Cylindrospermopsis raciborskii in New Zealand, New Zeal. J. Mar. Fresh. Res. 37: 821–828.

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