Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-26T20:58:51.077Z Has data issue: false hasContentIssue false

First report of neurotoxic effect of the cyanobacterium Cylindrospermopsis raciborskii on the motility of trematode metacercariae

Published online by Cambridge University Press:  28 March 2017

K.C. Lopes
Affiliation:
Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil, 4365 – Manguinhos, Rio de Janeiro – RJ, 21040–360, Brazil Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil
A.S. Ferrão-Filho
Affiliation:
Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil, 4365 – Manguinhos, Rio de Janeiro – RJ, 21040–360, Brazil
E.G.N. Santos
Affiliation:
Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil, 4365 – Manguinhos, Rio de Janeiro – RJ, 21040–360, Brazil Fundação Instituto de Pesca do Estado do Rio de Janeiro – FIPERJ, Escritório Regional Metropolitano II, Duque de Caxias, – RJ, 25071-160, Brazil
C.P. Santos*
Affiliation:
Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil, 4365 – Manguinhos, Rio de Janeiro – RJ, 21040–360, Brazil

Abstract

Cylindrospermopsis raciborskii (Woloszynska) is a photosynthetic cyanobacterium that can produce cytotoxic (cylindrospermopsin) and neurotoxic cyanotoxins (saxitoxins). In Brazil the strains of C. raciborskii are reported to produce only saxitoxins (STX) and their effect on fish parasites has not been tested to date. The fish Poecilia vivipara Bloch and Schneider is a common host for the trematode Pygidiopsis macrostomum Travassos off the coast of Rio de Janeiro, and this fish–parasite interaction is a model for behavioural and ecotoxicological studies. The aim of this work was to evaluate the motility of metacercariae of P. macrostomum from P. vivipara exposed to 40 mg l−1 and 400 mg l−1 of crude lyophilized extract of the cyanobacterium C. raciborskii (CYRF-01) for 48 h. The fish were separated into groups of ten individuals and, after exposure, five fish from each group were dissected for counting and checking the motility of metacercariae. The other five fish were dissected after 48 h in clean water. The detection and quantification of STX in the solutions of cyanobacteria, and the gills and guts of fish, were performed by an enzyme-linked immunosorbent assay. The crude extract of C. raciborskii caused temporary paralysis in metacercariae of P. macrostomum after exposure of fish to both concentrations, and the motility recovered after the fish were kept for 48 h in clean water. STX was detected in the guts and gills of all fish analysed, suggesting that this toxin is involved in the paralysis of metacercariae. This is the first report on the action of neurotoxins in metacercariae of fish.

Type
Short Communications
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beeby, A. (1999) What do sentinels stand for? Environmental Pollution 112, 285298.Google Scholar
Bieczynski, F., Bianchi, V.A. & Luquet, C.M. (2013) Accumulation and biochemical effects of microcystin-LR on Patagonian pejerrey (Odontesthes hatcheri) fed with the toxic cyanobacteria Microcystis aeruginosa . Fish Physiology and Biochemistry 39, 13091321.Google Scholar
Borges, J.N., Costa, V.S., Mantovani, C., Barros, E., Santos, E.G.N., Mafra, C.L. & Santos, C.P. (2017) Molecular characterization and confocal laser scanning microscopic study of Pygidiopsis macrostomum (Trematoda: Heterophyidae) parasites of guppies Poecilia vivipara . Journal of Fish Diseases 40, 191203.CrossRefGoogle ScholarPubMed
Chorus, I. & Bartram, J. (1999) Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management. London, E. & F.N. Spon.Google Scholar
Costa, P.R., Lage, S., Barata, M. & Ferreira, P.P. (2011) Uptake, transformation, and elimination kinetics of paralytic shellfish toxins in white seabream (Diplodus sargus). Marine Biology 158, 28052811.Google Scholar
Drobac, D., Tokodi, N., Lujić, J., Marinović, Z., Subakov-Simić, G., Dulić, T., Važić, T., Nybomd, S., Meriluoto, J., Codd, G.A. & Svirčev, Z. (2016) Cyanobacteria and cyanotoxins in fishponds and their effects on fish tissue. Harmful Algae 55, 6676.CrossRefGoogle ScholarPubMed
Etheridge, S.M. (2010) Paralytic shellfish poisoning: seafood safety and human health perspectives. Toxicon 56, 108122.CrossRefGoogle ScholarPubMed
Ferrão-Filho, A.S. & Kozlowsky-Suzuki, B. (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Marine Drugs 9, 27292772.Google Scholar
Ferrão-Filho, A.S., Cunha, R., Magalhães, V.F., Soares, M.C.S. & Baptista, D.F. (2007) Evaluation of sub-letal toxicity of cyanobacteria on the swimming activity of aquatic organisms by image analysis. Journal of the Brazilian Society of Ecotoxicology 2, 93100.CrossRefGoogle Scholar
Ferrão-Filho, A.S., Soares, M.C.S., Magalhães, V.F. & Azevedo, S.M.F.O. (2009) Biomonitoring of cyanotoxins in two tropical reservoirs by cladoceran toxicity bioassays. Ecotoxicology and Environmental Safety 72, 479489.CrossRefGoogle Scholar
Ferrão-Filho, A.S., Soares, M.C.S., Magalhães, V.F. & Azevedo, S.M.F.O. (2010) A rapid bioassay for detecting saxitoxins using a Daphnia acute toxicity test. Environmental Pollution 158, 20842093.CrossRefGoogle ScholarPubMed
Gorham, P.R., Mclachlav, J.R., Hammer, V.T. & Kim, W.K. (1964) Isolation and culture of toxic strains of Anabaena flos-aquae (Lyngb.) de Bréb. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 15, 796804.Google Scholar
Haney, J.F., Sasner, J.J. & Ikawa, M. (1995) Effects of products released by Aphanizomenon flos-aquae and purified saxitoxin on the movements of Daphnia carinata feeding appendages. Limnology and Oceanography 40, 263272.Google Scholar
Hudnell, H.K. (2008) Cyanobacterial harmful algal blooms: state of science and research needs. Advances in Experimental Medicine and Biology 619, 116.CrossRefGoogle ScholarPubMed
Ives, J.D. (1985) The relationship between Gonyaulax tamarensis cell toxin levels and copepod ingestion rate. pp. 413–418 in Anderson, D.M., White, A.W. & Baden, D.G. (Eds) Toxic dinoflagellates. New York, Elsevier.Google Scholar
Koblitz, J.L., Andreata, J.V. & Marca, A.G. (2001) Distribuição dos metais pesados nos sedimentos recentes da Laguna Rodrigo de Freitas, Rio de Janeiro, Brasil. pp. 290296 in Andreata, J.V. (Ed.) Lagoa Rodrigo de Freitas: síntese histórica e ecológica. Rio de Janeiro, Universidade Santa Úrsula.Google Scholar
Lee, R.E. (2008) Phycology. Cambridge, Cambridge University Press.Google Scholar
Lopes, K.C., Ferrão-Filho, A.S., Santos, E.G., Cunha, R.A. & Santos, C.P. (2017) Effects of crude extracts of a saxitoxin-producer strain of the cyanobacterium Cylindrospermopsis raciborskii on the swimming behavior of wild and laboratory reared guppy Poecilia vivipara . Toxicon 129, 4451.Google Scholar
Magalhães, V.F., Marinho, M.M., Domingos, P., Oliveira, A.C.P., Costa, S.M., Azevedo, L.O. & Azevedo, S.M.F.O. (2003) Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brazil, RJ). Toxicon 42, 289295.CrossRefGoogle Scholar
Marcogliese, D.J. (2004) Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35, 705716.Google Scholar
Mendonça, J.P. & Andreata, J.V. (2001) Aspectos reprodutivos de Poecilia vivipara (Bloch & Schneider) (Poeciliidae) da Lagoa Rodrigo de Freitas, Rio de Janeiro, Brasil. Revista Brasileira de Zoologia 18, 10411047.Google Scholar
Metcalf, J.S., Beattie, K.A., Pflugmacher, S. & Codd, G.A. (2000) Immuno-cross-reactivity and toxicity assessment of conjugation products of the cyanobacterial toxin, microcystin-LR. FEMS Microbiology Letters 189, 155158.Google Scholar
Metcalf, J.S., Beattie, K.A., Ressler, J., Gerbersdorf, S., Pflugmacher, S. & Codd, G.A. (2002) Cross-reactivity and performance assessment of four microcystin immunoassays with detoxification products of the cyanobacterial toxin, microcystin-LR. Journal of Water Supply: Research and Technology 51, 145151.Google Scholar
Ministry of Health, Brazil. (2004) Portaria n° 518, de 25 de março de 2004. Available at http://www.aeap.org.br/doc/portaria_518_de_25_de_marco_2004.pdf (accessed 15 August 2016).Google Scholar
Molica, R., Onodera, H., García, C., Rivas, M. & Andrinolo, D. (2002) Toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) isolated from Tabocas reservoir in Caruaru, Brazil, including demonstration of a new saxitoxin analogue. Phycologia 41, 606611.Google Scholar
Nogueira, I.C.G., Pereira, P., Dias, E., Pflumacher, S., Wiegand, C., Franca, S. & Vasconcelos, V.M. (2004) Accumulation of paralytic shellfish toxins (PST) from the cyanobacterium Aphanizomenon issatschenkoi by cladoceran Daphnia magna . Toxicon 44, 773780.Google Scholar
Pflugmacher, S., Wiegand, C., Oberemm, A., Beattie, K.A., Krause, E., Codd, G.A. & Steinberg, C.E.W. (1998) Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxication. Biochimica et Biophysica Acta – General Subjects 1425, 527533.Google Scholar
R Development Core Team. (2014) R. A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at http://www.R-project.org/ (accessed 10 March 2016).Google Scholar
Restani, G.C. & Fonseca, A.L. (2014) Effects of Cylindrospermopsis raciborskii strains (Woloszynska, 1912) Senayya & Subba Raju on the mobility of Daphnia laevis (Cladocera, Daphniidae). Brazilian Journal of Biology 74, 2331.Google Scholar
Romo, S., Soria, J., Fernandez, F., Ouahid, Y. & Baron-Sola, A. (2013) Water residence time and the dynamics of toxic cyanobacteria. Freshwater Biology 58, 513522.Google Scholar
Santos, E.G.N. & Santos, C.P. (2013) Parasite-induced and parasite development-dependent alteration of the swimming behavior of fish hosts. Acta Tropica 127, 5662.CrossRefGoogle ScholarPubMed
Santos, E.G.N., Cunha, R.A. & Santos, C.P. (2011) Behavioral responses of Poecilia vivipara (Osteichthyies: Cyprinodontiformes) to experimental infections of Acanthocollaritrema umbilicatum (Digenea: Cryptogonimidae). Experimental Parasitology 127, 522526.CrossRefGoogle ScholarPubMed
Simões, S.B.E., Barbosa, H.S. & Santos, C.P. (2005) Redescription and surface ultrastructure of Pygidiopsis macrostomum (Digenea: Heterophyidae). Journal of Parasitology 91, 931936.Google Scholar
Simões, S.B.E., Barbosa, H.S. & Santos, C.P. (2009) The life history of Pygidiopsis macrostomum Travassos, 1928 (Digenea: Heterophyidae). Memórias do Instituto Oswaldo Cruz 104, 106111.CrossRefGoogle ScholarPubMed
Sivonen, K. & Jones, G. (1999) Cyanobacterial toxins. pp. 41111 in Chorus, I. & Bartram, J. (Eds) Toxic cyanobacteria in water. A guide to their public health significance, monitoring and management. London, E. & F.N. Spon.Google Scholar
Sures, B. (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170177.Google Scholar
Teegarden, G.J. & Cembella, A.D. (1996) Grazing of toxic dinoflagellates, Alexandrium spp., by adult copepods of coastal Maine: implications for the fate of paralytic shellfish toxins in marine food webs. Journal of Experimental Marine Biology and Ecology 196, 145176.Google Scholar