Okadaic Acid Depuration from the Cockle Cerastoderma edule
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Biological Material and Experimental Design
4.2. Chemicals and Reference Materials
4.3. Toxin Extraction and Hydrolysis
4.4. LC-MS/MS Method
4.5. Modelling
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Lee, J.S.; Igarashi, T.; Fraga, S.; Dahl, E.; Hovgaard, P.; Yasumoto, T. Determination of diarrhetic shellfish toxins in various dinoflagellate species. J. Appl. Phycol. 1989, 1, 147–152. [Google Scholar] [CrossRef]
- Murakami, Y.; Oshima, Y.; Yasumoto, T. Identification of Okadaic Acid As a Toxic Component of a Marine Dinoflagellate Prorocentrum Lima. Nippon. Suisan Gakkaishi 1982, 48, 69–72. [Google Scholar] [CrossRef]
- Dickey, R.W.; Bobzin, S.C.; Faulkner, D.J.; Bencsath, F.A.; Andrzejewski, D. Identification of okadaic acid from a Caribbean dinoflagellate, Prorocentrum Concavum. Toxicon 1990, 28, 371–377. [Google Scholar] [CrossRef]
- Morton, S.L.; Moeller, P.D.R.; Young, K.A.; Lanoue, G. Okadaic acid production from the dinoflagellate Prorocentrum belizeanum Faust isolated from the Belizean coral reef ecosystem. Toxicon 1988, 36, 201–206. [Google Scholar] [CrossRef]
- Suzuki, T.; Beuzenberg, V.; Mackenzie, L.; Quilliam, M.A. Discovery of okadaic acid esters in the toxic dinoflagellate Dinophysis acuta from New Zealand using liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass. Spectrom. 2004, 18, 1131–1138. [Google Scholar] [CrossRef]
- Reguera, B.; Riobó, P.; Rodríguez, F.; Díaz, P.; Pizarro, G.; Paz, B.; Franco, J.; Blanco, J. Dinophysis Toxins: Causative Organisms, Distribution and Fate in Shellfish. Mar. Drugs 2014, 12, 394–461. [Google Scholar] [CrossRef]
- Paz, B.; Daranas, A.H.; Cruz, P.G.; Franco, J.M.; Norte, M.; Fernández, J.J. Identification of 19-epi-okadaic acid, a new diarrhetic shellfish poisoning toxin, by liquid chromatography with mass spectrometry detection. Mar. Drugs 2008, 6, 489–495. [Google Scholar]
- Miles, C.O.; Wilkins, A.L.; Hawkes, A.D.; Jensen, D.J.; Cooney, J.M.; Larsen, K.; Petersen, D.; Rise, F.; Beuzenberg, V.; MacKenzie, A.L. Isolation and identification of a cis-C-8-diol-ester of okadaic acid from Dinophysis acuta in New Zealand. Toxicon 2006, 48, 195–203. [Google Scholar] [CrossRef]
- Nielsen, L.T.; Krock, B.; Hansen, P.J. Production and excretion of okadaic acid, pectenotoxin-2 and a novel dinophysistoxin from the DSP-causing marine dinoflagellate Dinophysis acuta—Effects of light, food availability and growth phase. Harmful Algae 2013, 23, 34–45. [Google Scholar] [CrossRef]
- Hu, T.; Curtis, J.M.; Walter, J.A.; McLachlan, J.L.; Wright, J.L.C. Two new water-soluble dsp toxin derivatives from the dinoflagellate Prorocentrum maculosum: Possible storage and excretion products. Tetrahedron Lett. 1995, 36, 9273–9276. [Google Scholar] [CrossRef]
- Hu, T.; de Freitas, A.S.W.; Doyle, J.; Jackson, D.; Marr, J.; Nixon, E.; Pleasance, S.; Quilliam, M.A.; Walter, J.A.; Wright, J.L.C. New dsp toxin derivatives isolated from toxic mussels and the dinoflagellates, Prorocentrum lima and Prorocentrum concavum. Toxic Phytoplankton Bloom. Sea 1993, 3, 507–512. [Google Scholar]
- Yasumoto, T.; Oshima, Y.; Yamaguchi, M. Occurrence of a new type of shellfish poisoning in the Tohoku district. Bull. Jap. Soc. Sci. Fish. 1978, 44, 1249–1255. [Google Scholar] [CrossRef]
- EU. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for on the hygiene of foodstuffs. Off. J. Eur. Communities 2004, 139, 55–205. [Google Scholar]
- EFSA Panel on Contaminants in the Food Chain. Marine biotoxins in shellfish-okadaic acid and analogues-Scientific Opinion of the Panel on Contaminants in the Food chain. EFSA J. 2008, 6, 589. [Google Scholar] [CrossRef]
- Carss, D.N.; Brito, A.C.; Chainho, P.; Ciutat, A.; de Montaudouin, X.; Fernandez Otero, R.M.; Filgueira, M.I.; Garbutt, A.; Goedknegt, M.A.; Lynch, S.A.; et al. Ecosystem services provided by a non-cultured shellfish species: The common cockle Cerastoderma edule. Mar. Environ. Res. 2020, 158, 104931. [Google Scholar] [CrossRef] [PubMed]
- Pescadegalicia. Estatísticas. Publicacións. Available online: https://www.pescadegalicia.gal/gl/publicacions (accessed on 24 January 2022).
- Blanco, J. Accumulation of Dinophysis Toxins in Bivalve Molluscs. Toxins 2018, 10, 453. [Google Scholar] [CrossRef] [Green Version]
- Svensson, S.; André, C.; Rehnstam-Holm, A.S.; Hansson, J. A case of consistent spatial differences in content of diarrhetic shellfish toxins (DST) among three bivalve species: Mytilus edulis, Ostrea edulis and Cerastoderma edule. J. Shellfish. Res. 2000, 19, 1017–1020. [Google Scholar]
- Vale, P. Differential Dynamics of Dinophysistoxins and Pectenotoxins Between Blue Mussel and Common Cockle: A Phenomenon Originating From the Complex Toxin Profile of Dinophysis acuta. Toxicon 2004, 44, 123–134. [Google Scholar] [CrossRef]
- Blanco, J.; Fernández, M.L.; Míguez, A.; Moroño, A. Okadaic acid depuration in the mussel Mytilus galloprovincialis: One- and two-compartment models and the effect of environmental conditions. Mar. Ecol. Prog. Ser. 1999, 176, 153–163. [Google Scholar] [CrossRef]
- Fernández, M.L.; Míguez, A.; Moroño, A.; Cacho, E.; Martínez, A.; Blanco, J. Detoxification of low polarity toxins (DTX3) from mussels Mytilus galloprovincialis in Spain. In Harmful Algae; Reguera, B., Blanco, J., Fernández, M.L., Wyatt, T., Eds.; Xunta de Galicia and IOC of UNESCO: Santiago de Compostela, Spain, 1998; pp. 449–452. [Google Scholar]
- Moroño, A.; Arévalo, F.; Fernández, M.L.; Maneiro, J.; Pazos, Y.; Salgado, C.; Blanco, J. Accumulation and transformation of DSP toxins in mussels Mytilus galloprovincialis LMK during a toxic episode caused by Dinophysis acuminata. Aquat. Toxicol. 2003, 62, 269–280. [Google Scholar] [CrossRef]
- Moroño, A.; Fernández, M.L.; Franco, J.M.; Martínez, A.; Reyero, I.; Míguez, A.; Cacho, E.; Blanco, J. PSP and DSP detoxification kinetics in mussel, Mytilus galloprovincialis: Effect of environmental parameters and body weight. In Harmful Algae; Reguera, B., Blanco, J., Fernández, M.L., Wyatt, T., Eds.; Xunta de Galicia and IOC of UNESCO: Santiago de Compostela, Spain, 1998; pp. 445–448. [Google Scholar]
- Poletti, R.; Viviani, R.; Casadei, C.; Lucentini, L.; Giannetti, L.; Funari, E.; Draisci, R. Decontamination dynamics of mussels naturally contaminated with diarrhetic toxins relocated to a basin of the Adriatic Sea. In Harmful and Toxic Algal Blooms; Yasumoto, T., Oshima, Y., Fukuyo, Y., Eds.; IOC of UNESCO: Paris, France, 1996; pp. 429–432. [Google Scholar]
- Marcaillou-Le Baut, C.; Bardin, B.; Bardouil, M.; Bohec, M.; Le Dean, L.; Masselin, P.; Truquet, P. DSP depuration rates of mussels reared in a laboratory and an aquaculture pond. In Toxic Phytoplankton Blooms in the Sea; Smayda, T.J., Shimizu, Y., Eds.; Elsevier: New York, NY, USA; Amsterdam, The Netherlands, 1993; pp. 531–535. [Google Scholar]
- Botelho, M.J.; Vale, C.; Joaquim, S.; Costa, S.T.; Soares, F.; Roque, C.; Matias, D. Combined effect of temperature and nutritional regime on the elimination of the lipophilic toxin okadaic acid in the naturally contaminated wedge shell Donax trunculus. Chemosphere 2018, 190, 166–173. [Google Scholar] [CrossRef] [PubMed]
- Vale, P. Differential dynamics of dinophysistoxins and pectenotoxins, part II: Offshore bivalve species. Toxicon 2006, 47, 163–173. [Google Scholar] [CrossRef] [PubMed]
- Rossignoli, A.E.; Fernández, D.; Regueiro, J.; Mariño, C.; Blanco, J. Esterification of okadaic acid in the mussel Mytilus galloprovincialis. Toxicon 2011, 57, 712–720. [Google Scholar] [CrossRef]
- Janer, G.; Mesia-Vela, S.; Porte, C.; Kauffman, F.C. Esterification of vertebrate-type steroids in the Eastern oyster (Crassostrea virginica). Steroids 2004, 69, 129–136. [Google Scholar] [CrossRef]
- Torgersen, T.; Sandvik, M.; Lundve, B.; Lindegarth, S. Profiles and levels of fatty acid esters of okadaic acid group toxins and pectenotoxins during toxin depuration. Part II: Blue mussels (Mytilus edulis) and flat oyster (Ostrea edulis). Toxicon 2008, 52, 418–427. [Google Scholar] [CrossRef]
- Lindegarth, S.; Torgersen, T.; Lundve, B.; Sandvik, M. Differential Retention Of Okadaic Acid (Oa) Group Toxins And Pectenotoxins (Ptx) In The Blue Mussel, Mytilus edulis (L.), And European Flat Oyster, Ostrea Edulis (L.). J. Shellfish. Res. 2009, 28, 313–323. [Google Scholar] [CrossRef]
- Blanco, J.; Martín, H.; Mariño, C.; Rossignoli, A.E. Simple Diffusion as the Mechanism of Okadaic Acid Uptake by the Mussel Digestive Gland. Toxins 2019, 11, 395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Konoki, K.; Onoda, T.; Watanabe, R.; Cho, Y.; Kaga, S.; Suzuki, T.; Yotsu-Yamashita, M. In Vitro Acylation of Okadaic Acid in the Presence of Various Bivalves’ Extracts. Mar. Drugs 2013, 11, 300–315. [Google Scholar] [CrossRef] [Green Version]
- Blanco, J.; Arévalo, F.; Correa, J.; Moroño, A. Lipophilic Toxins in Galicia (NW Spain) between 2014 and 2017: Incidence on the Main Molluscan Species and Analysis of the Monitoring Efficiency. Toxins 2019, 11, 612. [Google Scholar] [CrossRef] [Green Version]
- Escudeiro Rossignoli, A. Acumulación de Toxinas DSP en el Mejillón Mytilus galloprovincialis. Ph.D. Thesis, Santiago de Compostela University, Santiago de Compostela, Spain, 2011. [Google Scholar]
- EURLMB. EU-Harmonised Standard Operating Procedure for Determination of Lipophilic Marine Biotoxins in Molluscs by LC-MS/MS, Version 5. 2014. Available online: https://www.aesan.gob.es/AECOSAN/docs/documentos/laboratorios/LNRBM/ARCHIVO2EU-Harmonised-SOP-LIPO-LCMSMS_Version5.pdf (accessed on 15 January 2022).
- Rossignoli, A.E.; Mariño, C.; Martín, H.; Blanco, J. Development of a Fast Liquid Chromatography Coupled to Mass Spectrometry Method (LC-MS/MS) to Determine Fourteen Lipophilic Shellfish Toxins Based on Fused–Core Technology: In-House Validation. Mar. Drugs 2021, 19, 603. [Google Scholar] [CrossRef]
- Gerssen, A.; Mulder, P.P.; McElhinney, M.A.; de Boer, J. Liquid chromatography–tandem mass spectrometry method for the detection of marine lipophilic toxins under alkaline conditions. J. Chromatogr. A 2009, 1216, 1421–1430. [Google Scholar] [CrossRef] [PubMed]
- R Core Team. R: A Language and Environment for Statistical Computing; Version 4.0.2; R Foundation for Statistical Computing: Vienna, Austria, 2020; Available online: https://www.R-project.org/ (accessed on 30 January 2022).
- Soetaert, K.; Petzoldt, T.; Setzer, R.W. Solving Differential Equations in R: Package deSolve. J. Stat. Softw. 2010, 33, 1–25. [Google Scholar] [CrossRef]
- Soetaert, K.; Petzoldt, T. Inverse Modelling, Sensitivity and Monte Carlo Analysis in R Using Package FME. J. Stat. Softw. 2010, 33, 1–28. [Google Scholar] [CrossRef] [Green Version]
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis; Springer: Berlin/Heidelberg, Germany, 2016; 260p. [Google Scholar]
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Blanco, J.; Martín, H.; Mariño, C.; Rossignoli, A.E. Okadaic Acid Depuration from the Cockle Cerastoderma edule. Toxins 2022, 14, 216. https://doi.org/10.3390/toxins14030216
Blanco J, Martín H, Mariño C, Rossignoli AE. Okadaic Acid Depuration from the Cockle Cerastoderma edule. Toxins. 2022; 14(3):216. https://doi.org/10.3390/toxins14030216
Chicago/Turabian StyleBlanco, Juan, Helena Martín, Carmen Mariño, and Araceli E. Rossignoli. 2022. "Okadaic Acid Depuration from the Cockle Cerastoderma edule" Toxins 14, no. 3: 216. https://doi.org/10.3390/toxins14030216