Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms

Marine Environmental Research

Volumn 76, Issue , 2012, Pages 97-107

  Faimali, Marco ^a   Giussani, Valentina ^a,b   Piazza, Veronica ^a   Garaventa, Francesca ^a   Corrà, Christian ^a   Asnaghi, Valentina ^b   Privitera, Davide ^b   Gallus, Lorenzo ^b   Cattaneo Vietti, Riccardo ^b   Mangialajo, Luisa ^c   Chiantore, Mariachiara ^b  

^a CNR   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c Laboratoire Environnement Marin Littoral   (France)

Author keywords

Ecotoxicity bioassays; Ostreopsis ovata; Palytoxin; Toxicity

Indexed keywords

ALARM THRESHOLDS; ALGAL CELLS; ARTEMIA SALINA; BENTHIC MICROALGAE; CELL CONCENTRATIONS; DICENTRARCHUS LABRAX; ECONOMIC CONCERNS; ECOTOXICOLOGICAL; GROWTH MEDIUM; MARINE ORGANISMS; MASS MORTALITY; MEDITERRANEAN SEA; MODEL ORGANISMS; OSTREOPSIS OVATA; OXYGEN DEPLETION; PALYTOXIN; SEA BASS; SEAWATER TEMPERATURE; SENSITIVE SPECIES; TOURIST AREAS; TOXIC EFFECT;

ALGAE; CELLS; DIAGNOSIS; INDUSTRIAL POISONS; MARINE BIOLOGY; SEAWATER; SODIUM; TOXICITY; WATER ANALYSIS;

CELL CULTURE;

ALGAL BLOOM; BIOASSAY; CRUSTACEAN; DINOFLAGELLATE; ECOTOXICOLOGY; FISH; TOXICITY; TOXICITY TEST; TOXIN;

ALGAL BLOOM; AMPHIBALANUS AMPHITRITE; ANIMAL TISSUE; ARTEMIA SALINA; ARTICLE; BENTHOS; CONTROLLED STUDY; CRUSTACEA; DINOFLAGELLATE; ECOTOXICITY; ECOTOXICOLOGY; EUROPEAN SEA BASS; FISH; JUVENILE ANIMAL; MARINE SPECIES; NONHUMAN; OSTREOPSIS OVATA; TEMPERATURE; TIGRIOPUS FULVUS;

ANIMALS; AQUATIC ORGANISMS; BASS; BIOLOGICAL ASSAY; CRUSTACEA; DINOFLAGELLIDA; HARMFUL ALGAL BLOOM; LETHAL DOSE 50; MARINE TOXINS; TEMPERATURE;

MEDITERRANEAN SEA;

ALGAE; AMPHIBALANUS; AMPHITRITE; ARTEMIA SALINA; CRUSTACEA; DICENTRARCHUS LABRAX; DINOPHYCEAE; INVERTEBRATA; OSTREOPSIS; OSTREOPSIS OVATA; SERRANIDAE; TIGRIOPUS FULVUS; VERTEBRATA;

EID: 84859003755     PISSN: 01411136     EISSN: 18790291     Source Type: Journal    
DOI: 10.1016/j.marenvres.2011.09.010     Document Type: Article

References (79)

1. Abatzopoulos T.J., Kappas I., Bossier P. Genetic characterization of Artemia tibetiana (Crustacea: Anostraca). Biological Journal of the Linnean Society 2002, 75:333-344.
2. Alcala C.C., Alcala L.C., Garth J.S., Yasumura D., Yasumoto T. Human fatality due to the ingestion of the crab Demania reynaudiithat contained a palytoxin-like toxin. Toxicon 1988, 26:105-107.
3. Aligizaki K., Nikolaidis G. The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the north Aegean sea, Greece. Harmful Algae 2006, 5:717-730.
4. Aligizaki K., Katikou P., Milandri A., Diogène J. Occurrence of palytoxin-group toxins in seafood and future strategies to complement the present state of the art. Toxicon 2011, 57(3):390-399.
5. Alvarez J., Pedrol A., Parro I., Goxenci J., De Torres M., Manzanera M., Planas C., Cosculluela G., Lopez A., Masó M., Vila M., Isalt R. Brote epidémico de sintomatología irritativa en Sant Andreu de Llavaneres:¿el origen está en el agua del mar?. XXIII Reunión de laSociedad Española de Epidemiología 1-5 November 2005, Las Palmas de Gran Canaria, Spain.
6. Arystarkhova E., Wetzel R.K., Asinovski M.K., Sweadner K.J. The γ subunit modulates Na+ and K+ affinity of the renal Na, K-ATPase. Journal of Biological Chemistry 1999, 274:33,183-33,185.
7. Artoxkit, M., 1990. Artemia toxicity screening test for estuarine and marine waters. Standard operational procedure, Creasel, Deinze, Belgium.
8. Ballantine D.L., Tosteson C.G., Bardales A.T. Population dynamics and toxicity of natural populations of benthic dinoflagellates in southwestern Puerto Rico. J. Exp. Mar. Biol. Ecol. 1988, 119:201-212.
9. Barroso Garcia P., Rueda de la Puerta P., Carrano T.P., Martinez P.M., Enriquez E.G. Brote con sintomas respiratorios en la provinciade Almeria por una posible exposicion a microalgas toxicas. Gac. Sanit. 2008, 22(6):578-584.
10. Brescianini C., Grillo C., Melchiorre N., Bertolotto R., Ferrari A., Vivaldi B., Icardi G., Gramaccioni L., Funari E., Scardala S. Ostreopsis ovata algal blooms affecting human health in Genova, Italy, 2005 and 2006. Eurosurveillance 2006, 11(36). http://www.eurosurveillance.org/ViewArticle.aspx?Article=3040pii=3040.
11. Casavola N., Troncone A., Rizzi E., Favale M.G., Bello G. Microalghe marine tossiche nella provincia di Bari: danni ambientali, ittiofaunistici, evidenze epidemiologiche. Rapporti ISTISAN 2005, 05(29):92-97.
12. Cereijido M., Contreras R.G., Shoshani L. Cell adhesion, polarity, and epithelia in the dawn of metazoans. Physiol. Rev. 2004, 84:1229-1262. 10.1152/physrev.00001.2004.
13. Choong A.M.F., Teo S.L.M., Leow J.L., Koh H.L., Ho P.C.L. A preliminary ecotoxicity study of pharmaceuticals in the marine environment. J. Toxicol. Environ. Health A 2006, 69(21):1959-1970.
14. Ciminiello P., Dell'Aversano C., Fattorusso E., Forino M., Magno G.S., Tartaglione L., Grillo C., Melchiorre N. The Genoa 2005 outbreak. Determination of putative palytoxin in Mediterranean Ostreopsis ovata by a new liquid chromatography tandem mass spectrometry method. Anal. Chem. 2006, 78:6153-6159.
15. Ciminiello P., Dell'Aversano C., Dello Iacovo E., Fattorusso E., Forino M., Grauso L., Tartaglione L., Guerrini F., Pistocchi R. Complex palytoxin-like profile of Ostreopsis ovata. Identification of four new ovatoxins by high-resolution liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 2010, 24:2735-2744.
16. Cortas N., Arnaout M., Salon J., Edelman I.S. Isoforms of Na, K-ATPase in Artemia salina: II. Tissue distribution and kinetic characterization. J. Membr. Biol. 1989, 108:187-195.
17. Deeds J.R., Schwartz M.D. Human risk associated with palytoxin exposure. Toxicon 2009, 10.1016/j.toxicon.2009.05.035.
18. EFSA panel on contaminants in the food chain (CONTAM) Scientific opinion on marine biotoxins in shellfish - palytoxin group. EFSA J. 2009, 7(12):1393-1431.
19. Faimali M., Modena M., Falugi C., Gallus L., Oliveri S., Franzoni M., Peruzzo M., Giacco E., Piazza V., Garaventa F., Magillo F., Greco G., Corra C. Comparison and complementarity of different tests for environmental monitoring. Mar. Environ. Res. 2006, 62(Suppl. S):S384-S385.
20. Faimali M., Garaventa F., Piazza V., Magillo F., Greco G., Corrà C., Giacco E., Gallus L., Falugi C. Swimming speed alteration of larvae of Balanus amphitrite as behavioural end-point for laboratory toxicological bioassays. Mar. Biol. 2006, 149:87-96.
21. Faraponova O., De Pascale D., Onorati F., Finoia M.G. Tigriopus fulvus (Copepoda, Harpacticoida) as a target species in biological assays. Meiofauna Marina 2005, 14:91-94.
22. Faust M.A., Morton S., Quod J.P. Further SEM study of marinedinoflagellates: the genus Ostreopsis (Dinophyceae). J. Phycol. 1996, 32:1053-1065.
23. Faust M.A. Three new Ostreopsis species (Dinophyceae): O. marinus sp. nov., O. belizeanus sp. nov., and O. caribbeanus sp. nov. Phycologia 1999, 38:92-99.
24. Finney D.J. Statistical Method in Biological Assay 1978, Charles Griffin & Co. Ltd, London, England, p. 508. third ed.
25. Fisher J.A., Baxter-Lowe L.A., Hokin L.E. Regulation of Na, K-ATPase biosynthesis in developing Artemia salina. J. Biol. Chem. 1986, 261:515-519.
26. Fukuyo Y. Taxonomical study on benthic dinoflagellates collected in coral reefs. Bull. Jpn. Soc. Sci. Fish. 1981, 47:967-978.
27. Gorbi S., Bocchetti R., Binelli A., Totti C., Cucchiari E., Accoroni S., Raffaelli F., Nanetti L., Vignini A., Mazzanti L., Regoli F., Ciminiello P., Fattorusso E., Bacchiocchi S., Graziosi T., Orletti R. Biological effects of palytoxin-like compounds from benthic microalga Ostreopsis ovata: a multibiomarkers approach with the mussels Mytilus galloprovincialis. Comparat. Biochem. Physiol. A 2010, 157:S15-S21.
28. Granéli, E., Ferreira, C.E.L., Yasumoto, T., Rodrigues, E., Neves, M.B., 21-25 October 2002. Sea urchins poisoning by the benthic dinoflagellate Ostreopsis ovata on the Brazilian coast. In: Proceedings of the 10th International Conference on Harmful Algae, St. Pete Beach, FL, USA.
29. Greco G., Corra C., Garaventa F., Chelossi E., Faimali M. Standardization of laboratory bioassays with Balanus amphitrite larvae for preliminary oil dispersants toxicological characterization. Chem. Ecol. 2006, 22(1):163-172.
30. Granéli, E., Vidyarathna, N.K., Funari, E., Cumaranatunga, R., 3-7 November 2008. Climate change and benthic dinoflagellates - the Ostreopsis ovata case. In: Proceedings of the 13th International Conference on Harmful Algae, Hong Kong, pp. 42.
31. Habermann E. Review article. Palytoxin acts through Na+/K+ ATPase. Toxicon 1989, 27:1175-1187.
32. Hashimoto Y., Satake M., Ishida S., Inoue A., Kan Y., Yasumoto T. Aluterin: a toxin of filefish, Alutera scripta, probably originating from a zoanthid, Palythoa tuberculosa. Bull. Jpn. Soc. Sci. Fish. 1969, 35:1086-1093.
33. Ito E., Yasumoto T. Toxicological studies on palytoxin and ostreocin-D administered to mice by three different routes. Toxicon 2009, 54:244-251.
34. Kühlbrandt W. Biology, structure and mechanism of P-typeATPases. Nat. Rev. Mol. Cell. Biol. 2004, 5:282-295.
35. Lam P.K.S., Wo K.T., Wu R.S.S. Effects of cadmium on the development and swimming behavior of barnacle larvae Balanus amphitrite Darwin. Environ. Toxicol. 2000, 15(1):8-13.
36. Lenoir S., Ten-Hage L., Turquet J., Quod J.P., Bernard C., Hennion M.C. First evidence of palytoxin analogues from an Ostreopsis mascarenensis (Dinophyceae) benthic bloom in southwestern Indian Ocean. J. Phycol. 2004, 40:1042-1051.
37. Lucu C., Towle D.W. (Na+, K+)-ATPase in gills of aquatic crustacea. Comp. Biochem. Physiol. A 2003, 135:195-214.
38. Makridis P., Vadstein O. Food size selectivity of Artemia franciscana at three developmental stages. J. Plankton Res. 1999, 21(11):2191-2201.
39. Malagoli D., Casarini L., Ottaviani E. Effects of the marine toxins okadaic acid and palytoxin on mussel phagocytosis. Fish Shellfish Immunol. 2008, 24:180-186.
40. Manganelli, M., Bogialli, S., Di Corcia, A., Mattei, D., Mattera, F., Scardala, S., Scenari, R., Stefanelli, M., Funari, E., May 27-29, 2007. Temperature effect on palytoxin production by cultures of Ostreopsis ovata. In: Proceedings of The International Symposium on Algal Toxins, Trieste, pp. 48.
41. Mangialajo L., Bertolotto R., Cattaneo-Vietti R., Chiantore M., Grillo C., Lemee R., Melchiorre N., Moretto P., Povero P., Ruggieri N. The toxic benthic dinoflagellate Ostreopsis ovata: quantification of proliferation along the coastline of Genoa, Italy. Mar. Pollut. Bull. 2008, 56:1209-1214.
42. Mangialajo L., Ganzin N., Accoroni S., Asnaghi V., Blanfuné A., Cabrini M., Cattaneo-Vietti R., Chavanon F., Chiantore M., Cohu S., Costa E., Fornasaro D., Grossel H., Marco-Miralles F., Masó M., Reñé A., Rossi A.M., Montserrat Sala M., Thibaut T., Totti C., Vila M., Lemée R. Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon 2011, 57:408-420.
43. Moore R.E., Scheuer P.J. Palytoxin: a new marine toxin from a coelenterate. Science 1971, 172:495-498.
44. Morton B.E., Fraser C.F., Thenawidjaja M. Potent inhibition of sperm motility by palytoxin. Exp. Cell Res. 1982, 140:261-265.
45. Munday R. Palytoxin toxicology: animal studies. Toxicon 2011, 57(3):470-477.
46. OECD Guideline for testing of chemicals no. 203, adopted 17/07/1992. Fish, acute toxicity test, pp. 1-9.
47. Onuma Y., Satake M., Ukena T., Roux J., Chanteau S., Rasolofonirina N., Ratsimaloto M., Naoki H., Yasumoto T. Identification of putative palytoxin as the cause of clupeotoxism. Toxicon 1999, 37:55-65.
48. Pane L., Giacco E., Corrà C., Greco G., Mariottini G., Varisco F., Faimali M. Ecotoxicological evaluation of harbour sediments using organisms from different trophic levels. J. Soils Sediments 2008, 8(2):74-79.
49. Pearce I., Marshall J.A., Hallegraeff G.M. Toxic epiphytic dinoflagellates from East Coast Tasmania, Australia. Harmful Algal Blooms 2000, Proceedings of the Ninth International Conference on Harmful Algal Blooms, Australia 7-11 February 2000, 54-57. Intergovernmental Oceanographic Commission of UNESCO, Hobart, Australia. G.M. Hallegraeff, S.I. Blackburn, C.J. Bolch, R.J. Lewis (Eds.).
50. Penna A., Vila M., Fraga S., Giacobbe M.G., Francesco A., Riobó P., Vernesi C. Characterization of Ostreopsis and Coolia (Dinophyceae) isolates in the western Mediterranean Sea based on morphology, toxicity and internal transcribed spacer 5.8s rDNA sequences. J. Phycol. 2005, 41:212-225.
51. Pistocchi R., Pezzolesi L., Guerrini F., Vanucci S., Dell'Aversano C., Fattorusso E. A review on the effects of environmental conditions on growth and toxin production of Ostreopsis ovata. Toxicon 2011, 57:421-428.
52. Ramos V., Vasconcelos V. Review: palytoxin and analogs: biological and ecological effects. Marine Drugs 2010, 8:2021-2037.
53. Rhodes J.A., Susuki T., Briggs L., Garthwaite I. Toxic marine epiphyte dinoflagellates, Ostreopsis siamensis and Coolia monotis (Dinophyceae) in New Zealand. N.Z.J. Mar. Freshw. Res. 2000, 33:371-383.
54. Rhodes L.L., Towers N., Briggs L., Munday R., Adamson J. Uptake of palytoxin-like compounds by shellfish fed Ostreopsis siamensis (Dinophyceae). N.Z.J. Mar. Fresh. Res. 2002, 36:631-636.
55. Rhodes L., Munday R., Heasman K., Briggs L., Holland P., Adamson J. Uptake of palytoxin-related compounds by shellfish and paddlecrabs. Proceedings of the Sixth International Conference of Molluscan Shellfish Safety, 18-23 March 2007, Blenheim, New Zealand 2008, 168-176. Royal Society of New Zealand. P. Busby (Ed.).
56. Rhodes L. World-wide occurrence of the toxic dinoflagellate genus Ostreopsis Schmidt. Toxicon 2011, 57(3):400-407.
57. Riobó P., Paz B., Franco J.M. Analysis of palytoxin-like in Ostreopsis cultures by liquid chromatography with precolumn derivatization and fluorescence detection. Anal. Chim. Acta 2006, 566:217-223.
58. Riobó P., Franco J.M. Palytoxins: biological and chemical determination. Toxicon 2011, 57:368-375.
59. Rossi R., Castellano V., Scalco E., Serpe L., Zingone A., Soprano V. New palytoxin-like molecules in Mediterranean Ostreopsis cf. ovata (Dinoflagellates) and in Palythoa tuberculosa detected by liquid chromatography-electrospray ionization time-of-flight mass spectrometry. Toxicon 2010, 56:1381-1387.
60. Rossini G.P., Bigiani A. Palytoxin action on the Na+, K+-ATPase and the disruption of ion equilibria in biological systems. Toxicon 2011, 57(3):429-439.
61. Sáez A.G., Lozano E., Zaldivar-Riveron A. Evolutionary history of Na, K-ATPases and their osmoregulatory role. Genetica 2009, 136:479-490.
62. Satoh E., Ishii T., Nishimura M. Palytoxin-induced increase in cytosolic-free Ca2+ in mouse spleen cells. Eur. J. Pharmacol. 2003, 465:9-13.
63. Shears N.T., Ross P.M. Blooms of benthic dinoflagellates of the genus Ostreopsis; an increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae 2009, 8:916-925.
64. Simoni F., Gaddi A., Di Paolo C., Lepri L., Mancino A., Falaschi A. Further investigation on blooms of Ostreopsis ovata, Coolia monotis, Prorocentrum lima on the macroalgae of artificial and natural reefs in the Northern Tyrrhenian Sea. Harmful Algae News 2004, 26:5-7.
65. Sun H., Gao J., Ferrington D.A., Biesiada H., Williams T.D., Squier T.C. Repair of oxidized calmodulin by methionine sulfoxide reductase restores ability to activate the plasma membrane Ca-ATPase. Biochemistry 1999, 38(1):105-112.
66. Taniyama S., Arakawa O., Terada M., Nishio S., Takatani T., Mahmud Y., Noguchi T. Ostreopsisspa possible origin of palytoxin (PTX) in parrotfish Scarus ovifrons. Toxicon 2003, 42:29-33.
67. Therien A.G., Blostein R. Mechanisms of sodium pump regulation. Am. J. Physiol. Cell Physiol. 2000, 279:C541-C566.
68. Tognetto L., Bellato S., Moro I., Andreoli C. Occurrence of Ostreopsis ovata (Dinophyceae) in the Tyrrhenian Sea during summer 1994. Bot. Mar. 1995, 38:291-295.
69. Totti C., Accoroni S., Cerino F., Cucchiari E., Romagnoli T. Ostreopsis ovata bloom along the Conero Riviera (northern Adriatic Sea): relationships with environmental conditions and substrata. Harmful Algae 2010, 9:233-239.
70. Tubaro A., Durando P., Del Favero G., Ansaldi F., Icardi G., Deeds J.R., Sosa S. Case definitions for human poisonings postulated to palytoxins exposure. Toxicon 2011, 57(3):478-495.
71. Ukena T., Satake M., Usami M., Oshima Y., Naoki H., Fujita T., Kan Y., Yasumoto T. Structure elucidation of ostreocin D, a palytoxin analog isolated from the dinoflagellate Ostreopsis siamensis. Biosci. Biotechnol. Biochem. 2001, 65:2585-2588.
72. Usami M., Satake M., Ishida S., Inoue A., Kan Y., Yasumoto T. Palytoxin analogs from the dinoflagellate Ostreopsis siamensis. J. Am.Chem. Soc. 1995, 117:5389-5390.
73. Van Dolah F.M. Marine algal toxins: origins, health effects, and their increased occurrence. Environ. Health Perspect. 2000, 108(Suppl. 1):133-138.
74. Vale C., Ares I.R. Biochemistry of palytoxins and ostreocins. Phycotoxins, chemistry and biochemistry 2007, 95-118. Blackwell Publishing, Ames, IA, USA. L.M. Botana (Ed.).
75. Valverde I., Lago J., Reboreda A., Vieites J.M., Cabado A.G. Characteristics of palytoxin-induced cytotoxicity in neuroblastoma cells. Toxicol. In Vitro 2008, 22:1432-1439.
76. Vila M., Garcés E., Masó M. Potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat. Microb. Ecol. 2001, 26:51-60.
77. Vila, M., Masó, M., Sampedro, N., Illoul, H., Arin, L., Garcés, E., Giacobbe, M.G., Alvarez, J., Camp, J., 2008. The genus Ostreopsis in the recreational waters along the Catalan Coast and Balearic Islands (NW Mediterranean Sea): are they the origin of human respiratory difficulties? In: Proceedings of the 12th International Conference on Harmful Algae, pp. 334-336.
78. Wu R.S.S., Lam P.K.S., Zhou B.S. Effects of two oil dispersants on phototaxis and swimming behaviour of barnacle larvae. Hydrobiologia 1997, 352:9-16.
79. Wu C.H. Palytoxin: membrane mechanism of action. Toxicon 2009, 54:1183-1189.