Simultaneous accumulation of anatoxin-a and microcystins in three fish species indigenous to lakes affected by cyanobacterial blooms

Pawlik-Skowrońska, Barbara; Toporowska, Magdalena; Rechulicz, Jacek

doi:10.2478/s13545-012-0039-6

Abstract

A four-year study carried out in a lake with perennial water blooms caused by toxigenic Planktothrix agardhii (Oscillatoriales) and Anabaena lemmermanii, Anabaena flos-aquae, Anabaena spp. and Aphanizomenon issatchenkoi (Nostocales) revealed that the lake-dwelling fish were threatened by simultaneous exposure to intracellular and extracellular microcystins (MCs) as well as anatoxin-a (ANTX). Higher contents of anatoxin-a and microcystins were found in livers than in fish muscles. This is the first report on ANTX accumulation in the common fish, indigenous to European freshwaters during perennial cyanobacterial blooms. Generally, the omnivorous roach (Rutilus rutilus) and Prussian carp (Carassius gibelio) accumulated higher amounts of MCs in their tissues compared to mostly predacious perch (Perca fluviatilis), and similar amounts of ANTX. The long-lasting presence of MCs exceeding the safe levels for consumption was found in fish muscles. ANTX accumulation in fish muscles (up to 30 ng g−1 FW) suggests the probability of its transfer in a food chain.

References

[1] Adamovsky O., Kopp R., Hilscherova K., Babica P., Palikova M., Paskova V., Navratil S., Marsalek B., Blaha L., 2007, Microcystin kinetics ( bioaccumulation and elimination) and biochemical responses in common carp (Cyprinus carpio) and silver carp (Hypophthalmichthys molitrix) exposed to toxic cyanobacterial blooms. Environ. Toxicol. Chem. 26: 2687–2693. http://dx.doi.org/10.1897/07-213.110.1897/07-213.1
Search in Google Scholar
[2] Ballot A., Fastner J., Lantz M., Wiedner C., 2010, First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatchenkoi in northeastern Germany. Toxicon, 56: 964–971 http://dx.doi.org/10.1016/j.toxicon.2010.06.02110.1016/j.toxicon.2010.06.021
Search in Google Scholar
[3] Becker V., de Cardoso L., Motta Marques D., 2004, Development of Anabaena Bory ex Bornet & Flahault (Cyanobacteria) blooms in a shallow, subtropical lake in southern Brazil, Acta Limnol. Bras., 16: 306–317
Search in Google Scholar
[4] Berry J.P., Gantar M., Gibbs P.D., Schmale M.C. 2007, The zebrafish (Danio rerio) embryo as a model system for identification and characterization of developmental toxins from marine and freshwater microalgae, Comp. Bioch. Physiol. Part C, 145: 61–72 10.1016/j.cbpc.2006.07.011
Search in Google Scholar
[5] Bogialli S., Bruno M., Curini R., Di Corcia A., Lagana A., 2006, Simple and rapid determination of anatoxin-a in Lake water and Fish muscle tissue by liquid chromatography-tandem mass spectrometry, J. Chromatogr.A., 1122:180–185 http://dx.doi.org/10.1016/j.chroma.2006.04.06410.1016/j.chroma.2006.04.064
Search in Google Scholar
[6] Bradburn M., Lewis Jr W.M., McCutchan Jr J.H., 2012, Comparative adaptations of Aphanizpmenon and Anabaena for nitrogen fixation under weak irradiance. Freshwat. Biol., 57: 1042–1049. http://dx.doi.org/10.1111/j.1365-2427.2012.02765.x10.1111/j.1365-2427.2012.02765.x
Search in Google Scholar
[7] Briand J.F., Robillot C., Quiblier-Lloberas C., Bernard C., 2002, A perennial bloom of Planktothrix agardhii (Cyanobacteria) in a shallow eutrophic French lake: limnological and microcystin production studies Arch. Hydrobiol., 153: 605–622 10.1127/archiv-hydrobiol/153/2002/605
Search in Google Scholar
[8] Bumke-Vogt C., Mailahn W., Chorus I., 1999, Anatoxin-a and neurotoxic Cyanobacteria in German lakes and reservoirs., Environ. Toxicol., 14: 117–125 http://dx.doi.org/10.1002/(SICI)1522-7278(199902)14:1<;117::AID-TOX15>3.0.CO;2-V10.1002/(SICI)1522-7278(199902)14:1<;117::AID-TOX15>3.0.CO;2-V
Search in Google Scholar
[9] Carmichael W.W., 1992, Cyanobacteria secondary metabolites — the cyanotoxins. J. Appl. Bacteriol., 72: 445–459 http://dx.doi.org/10.1111/j.1365-2672.1992.tb01858.x10.1111/j.1365-2672.1992.tb01858.x
Search in Google Scholar
[10] Carlson R.E., 1977, A trophic state index for lakes, Limnol. Oceanogr., 22: 361–369 http://dx.doi.org/10.4319/lo.1977.22.2.036110.4319/lo.1977.22.2.0361
Search in Google Scholar
[11] Cazenave J., Bistoni M.A., Pesce S.F., Wunderlin D.A., 2006, Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus experimentally exposed to microcystin-RR, Aquat. Toxicol., 76: 1–12 http://dx.doi.org/10.1016/j.aquatox.2005.08.01110.1016/j.aquatox.2005.08.011
Search in Google Scholar
[12] Chen J., Xie P., Li L., Xu J., 2009, First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage, Toxicol. Sci., 108: 81–89 http://dx.doi.org/10.1093/toxsci/kfp00910.1093/toxsci/kfp009
Search in Google Scholar
[13] Codd, G., 2000, Cyanobacterial toxins, the parception of water quality, and the prioritisation of eutrophication control, Ecol. Eng., 16: 51–60 http://dx.doi.org/10.1016/S0925-8574(00)00089-610.1016/S0925-8574(00)00089-6
Search in Google Scholar
[14] Dikkeboom R., Van der Knaap W.P.W., Meuleman E.A., Sminia T., 1985, A comparative study on the internal defence system of juvenile and adult Lymnaea stagnalis, Immunology, 55: 547–553
Search in Google Scholar
[15] El Ghazali I., Saqrane S., Carvalho A.P., Ouahid Y., Del Campo F., Oudra B., Vasconcelos V., 2010, Effect of different microcystin profiles on toxin bioaccumulation in common carp (Cyprinus carpio) larvae via Artemia nauplii, Ecotox. Environ. Safety, 73: 762–770 http://dx.doi.org/10.1016/j.ecoenv.2009.12.01510.1016/j.ecoenv.2009.12.015
Search in Google Scholar
[16] Furey A., Crowley J., Hamilton B., Lehane M., James K.J., 2005, Strategies to avoid the mis-identification of anatoxin-a using mass spectrometry in the forensic investigation of acute neurotoxic poisoning, J. Chromat. A., 1082: 91–97 http://dx.doi.org/10.1016/j.chroma.2005.05.04010.1016/j.chroma.2005.05.040
Search in Google Scholar
[17] Golterman H.L., 1971, Methods for chemical analysis of fresh waters. Blackwell, IBP Handbook, Oxford, -, Edinburgh, pp. 166
Search in Google Scholar
[18] Grabowska M., Mazur-Marzec H., 2010, The effect of cyanobacterial blooms in the Siemianówka dam reservoir on the phytoplankton structure in the Narew river, Hydrobiol. Oceanol. Stud., 40:19–26 http://dx.doi.org/10.2478/s13545-011-0003-x10.2478/s13545-011-0003-x
Search in Google Scholar
[19] Harada K.I., Tsuji K., Watanabe M.F., Kondo F., 1996, Stability of microcystins from cyanobacteria. III. Effect of pH and temperature, Phycologia, 35: 83–88 http://dx.doi.org/10.2216/i0031-8884-35-6S-83.110.2216/i0031-8884-35-6S-83.1
Search in Google Scholar
[20] Hardy J., 2008, Final Report. Washington State Recreational Guidance for Microcystins (Provisional) and Anatoxin-a (Interim/Provisional), Washington State Department of Health, Olympia, Washington, pp 19
Search in Google Scholar
[21] Ibelings B.W., Bruning K., de Jonge J., Wolfstein K., Dionisio Pires L., Postma J., Burger T., 2005, Distribution of microcystins in a lake foodweb: no evidence for biomagnification, Microbial. Ecol., 49: 487–500 http://dx.doi.org/10.1007/s00248-004-0014-x10.1007/s00248-004-0014-x
Search in Google Scholar
[22] James K.J., Furey A., Sherlock I.R., Stack M.A., Twohing M., 1998, Sensitive determination of anatoxin-a, homoanatoxin-a and their degradation products by liquid chromatography with fluorometric detection, J. Chromatogr. A., 798: 147–157 http://dx.doi.org/10.1016/S0021-9673(97)01207-710.1016/S0021-9673(97)01207-7
Search in Google Scholar
[23] Kaya K., Sano T., 1999, Total microcystin determination using erythro-2-methyl-3-(methoxy-d3)-4-phenylbutyric acid (MMPB-d3) as the internal standard, Anal. Chim. Acta., 386: 107–112 http://dx.doi.org/10.1016/S0003-2670(99)00012-410.1016/S0003-2670(99)00012-4
Search in Google Scholar
[24] Kopp R., Mareš J., Palíková M., Navrátil S., Kubíček Z., Ziková A., Klávková J., Bláha L., 2009, Biochemical parameters of blood plasma and content of microcystins in tissues of common carp (Cyprinus carpio L.) from a hypertrophic pond with cyanobacterial water bloom, Aquacult. Res., 40: 1683–1693 http://dx.doi.org/10.1111/j.1365-2109.2009.02285.x10.1111/j.1365-2109.2009.02285.x
Search in Google Scholar
[25] Kamjunke N., Schmidt K., Pfchlugmacher S., Mehner T., 2002, Consumption of cyanobacteria by roach (Rutilus rutilus): useful or harmful to the fish?, Freshwat. Biol., 47: 243–250 http://dx.doi.org/10.1046/j.1365-2427.2002.00800.x10.1046/j.1365-2427.2002.00800.x
Search in Google Scholar
[26] Kolmakov V.I., Gladyshev M.I., 2003, Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crucian carp, Aquat. Ecol., 37: 237–242 http://dx.doi.org/10.1023/A:102580132608810.1023/A:1025801326088
Search in Google Scholar
[27] Kotak B.G., Zurawell R.W., Prepas E.E., Holmes C.F.B., 1996, Microcystin-LR concentration in aquatic food web compartments from lakes of varying trophic status, Can. J. Fish. Aquat. Sci., 53: 1974–1985 http://dx.doi.org/10.1139/cjfas-53-9-197410.1139/cjfas-53-9-1974
Search in Google Scholar
[28] Kurmayer R., Christiansen G., Fastner.J, Borner T., 2004, Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium Planktothrix spp, Environ. Microbiol., 6: 831–841 http://dx.doi.org/10.1111/j.1462-2920.2004.00626.x10.1111/j.1462-2920.2004.00626.x
Search in Google Scholar
[29] Lance E., Brient L., Bormans M., Gérard C., 2006, Interactions between cyanobacteria and Gastropods I. Ingestion of toxic Planktothrix agardhii by Lymnaea stagnalis and the kinetics of microcystin bioaccumulation and detoxification, Aquat. Toxicol., 79: 140–148 http://dx.doi.org/10.1016/j.aquatox.2006.06.00410.1016/j.aquatox.2006.06.004
Search in Google Scholar
[30] Lawton L.A., Edwards C., Codd G.A., 1994, Extraction and high performance liquid chromatographic method for the determination of microcystins in raw and treated waters, Analyst, 119: 1525–1530 http://dx.doi.org/10.1039/an994190152510.1039/an9941901525
Search in Google Scholar
[31] Li X.Y., Chung I.K., Kim J.I., Lee J.A., 2004, Subchronic oral toxicity of microcystin in common carp (Cyprinus carpio L.) exposed to Microcystis under laboratory conditions, Toxicon 44: 821–827 http://dx.doi.org/10.1016/j.toxicon.2004.06.01010.1016/j.toxicon.2004.06.010
Search in Google Scholar
[32] Malbrouck C., Kestemont P., 2006, Effects of microcystins on fish, Environ. Toxicol. Chem., 25: 72–86 http://dx.doi.org/10.1897/05-029R.110.1897/05-029R.1
Search in Google Scholar
[33] Mazur-Marzec H., 2006, Characterization of phycotoxins produced by Cyanobacteria, Oceanol. Hydrobiol. Stud., 35: 85–109
Search in Google Scholar
[34] Oberemm A., Fastner J., Steinberg C.E.W., 1997. Effects of microcystin-LR and cyanobacterial crude extracts on embryo-larval development of zebrafish (Danio rerio), Wat. Res., 11: 2918–2921 http://dx.doi.org/10.1016/S0043-1354(97)00120-610.1016/S0043-1354(97)00120-6
Search in Google Scholar
[35] Osswald J., Azevedo J., Vasconcelos V., Guilhermino L., 2011, Experimental determination of the bioconcentration factors for anatoxin-a in juvenile rainbow trout (Oncorhynchus mykiss). Proc. Intern.Ac. Ecol. Environ. Sci., 1(2): 77–86
Search in Google Scholar
[36] Osswald J, Carvalho A, Claro J., Vasconcelos V., 2009a, Effects of cyanobacterial extracts containing anatoxin-a and of pure anatoxin-a on early developmental stages of carp. Ecotoxicology and Environmental Safety, 72: 473–478 http://dx.doi.org/10.1016/j.ecoenv.2008.05.01110.1016/j.ecoenv.2008.05.01118640721
Search in Google Scholar
[37] Osswald J., Rellan S., Gago-Martinez A., Vasconcelos V., 2009b, Production of anatoxin-a by cyanobacterial strains isolated from Portugese fresh water systems, Ecotoxicology, 18: 1100–1115 http://dx.doi.org/10.1007/s10646-009-0375-510.1007/s10646-009-0375-5
Search in Google Scholar
[38] Osswald J., Rellán S., Carvalho A.P., Gago A., Vasconcelos V., 2007, Acute effects of an anatoxin-a producing cyanobacterium on juvenile fish — Cyprinus carpio L, Toxicon, 49: 693–698 http://dx.doi.org/10.1016/j.toxicon.2006.11.01010.1016/j.toxicon.2006.11.010
Search in Google Scholar
[39] Ozawa K., Yokoyama A., Ishikawa K., Kumagai M., Watanabe M.F., Park H.D., 2003, Accumulation and depuration of microcystin produced by the cyanobacterium Microcystis in a freshwater snail, Limnology, 4: 131–138 http://dx.doi.org/10.1007/s10201-003-0106-110.1007/s10201-003-0106-1
Search in Google Scholar
[40] Papadimitriou O., Kagalou I., Bacopoulos V., Leonardos I., 2010, Accumulation of microcystins in water and fish tissues: an estimation of risks associated with microcystins in most of the Greek lakes, Environ. Toxicol., 25: 418–427 http://dx.doi.org/10.1002/tox.2051310.1002/tox.20513
Search in Google Scholar
[41] Pawlik-Skowrońska B., Pirszel J., Kornijów R., 2008, Spatial and temporal variation in microcystin concentrations during perennial bloom of Planktothrix agardhiii in a hypertrophic lake, Ann. Limnol. — Int. J. Lim., 44: 63–68 http://dx.doi.org/10.1051/limn:200802310.1051/limn:2008023
Search in Google Scholar
[42] Pawlik-Skowrońska B., Skowroński T., Pirszel J., Adamczyk A., 2004, Relationship between cyanobacterial bloom and anatoxin-a and microcystin occurrence in the eutrophic dam reservoir (SE Poland), Pol. J. Ecol., 52: 479–490
Search in Google Scholar
[43] Pawlik-Skowrońska B., Toporowska M., 2011, Blooms of toxin-producing Cyanobacteria — a real threat in small dam reservoirs at the beginning of their operation, Hydrobiol. Oceanol. Stud., 40(4): 30–37 http://dx.doi.org/10.2478/s13545-011-0038-z10.2478/s13545-011-0038-z
Search in Google Scholar
[44] Pflugmacher S., Wiegand C., Oberemm A., Beattie K.A., Krause E., Codd G.A., 1998, Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxification, Biochim. Biophys. Acta., 142: 527–533 http://dx.doi.org/10.1016/S0304-4165(98)00107-X10.1016/S0304-4165(98)00107-X
Search in Google Scholar
[45] Rücker J., Wiedner C., Zippel P., 1997, Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes, Hydrobiologia, 342/343: 107–115 http://dx.doi.org/10.1023/A:101701320803910.1023/A:1017013208039
Search in Google Scholar
[46] Rantala-Ylinen A., Kana S., Wang H, Rouhiainen L., Wahlsten M., Rizzi E., Berg K., Gugger M., Sivonen K., 2011, Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. Strain 37 and molecular methods to detect potential producers. Appl. Environ. Microbiol., 77: 7271–7278 http://dx.doi.org/10.1128/AEM.06022-1110.1128/AEM.06022-11319486621873484
Search in Google Scholar
[47] Rymuszka A., Sierosławska A., 2010, Study on apoptotic effects of neurotoxin anatoxin-a on fish immune cells, Neuro. Endocrinol. Lett., 31Suppl. 2: 11–15
Search in Google Scholar
[48] Sivonen K., Himberg K., Luukkainen R., Niemela S.I., Poon G.K., Codd G.A., 1989, Preliminary Characterization of neurotoxic cyanobacteria blooms and strains from Finland, Toxicol. Assess., 4: 339–352 http://dx.doi.org/10.1002/tox.254004031010.1002/tox.2540040310
Search in Google Scholar
[49] Sivonen K., Niemelä S.I., Niemi R.M., Lepistö L., Luoma T.H., Räsänen L.A., 1990, Toxic cyanobacteria (blue-green algae) in Finnish fresh and coastal waters, Hydrobiologia, 190: 267–275 http://dx.doi.org/10.1007/BF0000819510.1007/BF00008195
Search in Google Scholar
[50] Smith et al. 2008
Search in Google Scholar
[51] Sotero-Santos R.B., Dellamano-Oliveira M.J., Carvalho E.G., Rocha O., 2008, Composition and toxicity of cyanobacterial bloom in a tropical reservoir. Harmful Algae, 7/5: 590–598 http://dx.doi.org/10.1016/j.hal.2007.12.01710.1016/j.hal.2007.12.017
Search in Google Scholar
[52] Toporowska M., Pawlik-Skowrońska B., Krupa D., Kornijów R., 2010, Winter versus summer blooming of phytoplankton in a shallow lake: effect of hypertrophic conditions, Pol. J. Ecol., 58: 159–168
Search in Google Scholar
[53] Utermöhl H., 1958, Zur Vervollkommung der quantitative Phytoplanktonmethodik, Mitt. Internat. Verein. Limnol., 2: 1–38 10.1080/05384680.1958.11904091
Search in Google Scholar
[54] Van Apeldoorn M.E., van Egmond H.P., Speijers G.J.A., Bakker G.J.I., 2007, Toxins of cyanobacteria. A review, Mol. Nutr. Food Res., 51: 7–60 http://dx.doi.org/10.1002/mnfr.20060018510.1002/mnfr.20060018517195276
Search in Google Scholar
[55] Welker M., Döhren H., 2006, Cyanobacterial peptides — nature’s own combinatorial biosynthesis, FEMS Microbiol. Rev., 30: 530–563 http://dx.doi.org/10.1111/j.1574-6976.2006.00022.x10.1111/j.1574-6976.2006.00022.x16774586
Search in Google Scholar
[56] WHO, 1999, Toxic Cyanobacteria in Water: A guide to their public health consequences, monitoring and management, Routledge London and New York
Search in Google Scholar
[57] Wilson A.E., Sarnelle O., Tillmanns A.R., 2006, Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments, Limnol. Oceanogr., 51: 1915–1924 http://dx.doi.org/10.4319/lo.2006.51.4.191510.4319/lo.2006.51.4.1915
Search in Google Scholar
[58] Zhang D., Xie P., Chen Y., Dai M., Qiu T., Liu Y., Liang G., 2009, Determination of microcystin-LR and its metabolites in snail (Bellemya aeruginosa), shrimp (Macrobrachium nipponensis) and silver carp (Hypophthalmichthys molitrix) from lake Taihu, China, Chemosphere, 76: 974–981 http://dx.doi.org/10.1016/j.chemosphere.2009.04.03410.1016/j.chemosphere.2009.04.03419473685
Search in Google Scholar
[59] Xie L.Q., Xie P., Guo L.G., Li L., Miyabara Y., Park H.D., 2005, Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China, Environ. Toxicol., 20: 293–300 http://dx.doi.org/10.1002/tox.2012010.1002/tox.2012015892067
Search in Google Scholar
[60] Xie L., Xie P., Ozawa K., Honma T., Yokoyama A., Park H-D., 2004, Dynamics of microcystins-LR and _RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environ. Pollut. 127: 431–439 http://dx.doi.org/10.1016/j.envpol.2003.08.01110.1016/j.envpol.2003.08.01114638304
Search in Google Scholar

Simultaneous accumulation of anatoxin-a and microcystins in three fish species indigenous to lakes affected by cyanobacterial blooms

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