Skip to main content
Log in

The seasonal dynamics of diarrhetic shellfish poisoning toxins in the digestive gland of Crenomytilus grayanus (Dunker, 1853) analyzed by high-performance liquid chromatography with fluorometric detection

  • Biochemistry
  • Published:
Russian Journal of Marine Biology Aims and scope Submit manuscript

Abstract

The seasonal dynamics of diarrhetic shellfish poisoning (DSP) toxins in the digestive gland of the mussel Crenomytilus grayanus (Dunker, 1853) from Peter the Great Bay in the Sea of Japan have been studied. Toxins in the form of 4-bromomethyl-7-methoxycoumarin derivatives have been analyzed using high-performance liquid chromatography (HPLC) with fluorometric detection. This method allows the determination of the quantitative and qualitative composition of individual toxins. All the C. grayanus samples contained DSP toxins, but their concentration varied substantially during the year. The highest concentration was recorded from the mussels collected in May; the lowest concentration was recorded in February. The toxins were represented predominantly by dinophysistoxin-2; in July-September and December, okadaic acid was detected. An assumption has been made about the relationship between the potential producers of DSP toxins in the waters of the Peter the Great Bay and the dynamics of these toxins in tissues of C. grayanus. The HPLC method, as an alternative to the enzyme-linked immunosorbent assay, was used to assess the quantitative and qualitative composition of DSP toxins in seafood for the first time in the Russian Federation. This method can be recommended for the routine monitoring of toxins conducted by the controlling organizations of the Russian Federal Service for Veterinary and Phytosanitary Surveillance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Yedinye sanitarno-epidemiologicheskiye i gigienicheskiye trebovaniya k produktsii (tovaram), podlezhashchei sanitarno- epidemiologicheskomu nadzoru (kontrolyu) (s izmeneniyami na 10 noyabrya 2015 goda): utv. resheniem Komissii Tamozhennogo Soyuza ot 28.05.2010 g. N 299. (Uniform Sanitary, Epidemiological, and Hygienic Requirements to the Product (Goods) Subject to Sanitary and Epidemiologic Supervision (Control) (with amendments on November 10, 2015), Approved by Decision of the Customs Union Commission, May 28, 2010, no. 299).

  2. Konovalova, G.V., Dinoflagellyaty (Dinophyta) dal’nevostochnykh morei Rossii i sopredel’nykh akvatorii Tikhogo okeana (Dinoflagellates (Dinophyta) in the Far Eastern Seas of Russia and Adjacent Waters of the Pacific Ocean), Vladivostok: Dal’nauka, 1998.

    Google Scholar 

  3. Kokhanova, Yu.A. and Khotimchenko, S.A., Biosafety: phytotoxins (part 3), Vopr. Pitaniya, 2006, no. 4, pp. 16–19.

    Google Scholar 

  4. Orlova, T.Yu., Monitoring of toxic microalgae as a basis for the biological safety of coastal waters and seafood, in Materialy Tselevoi kompleksnoi programmy orientirovannykh fundamental’nykh nauchnykh issledovanii Dal’nevostochnogo otdeleniya Rossiiskoi Akademii Nauk na 2007–2012 gg.: “Biologicheskaya bezopasnost’ dal’nevostochnykh morei Rossiiskoi Federatsii” (Materials of the Target Complex Program Oriented to the Fundamental Researches at the Far Eastern Branch, Russian Academy of Sciences for 2007–2012: “Biological Safety of the Far Eastern Seas of the Russian Federation”), Adrianov, A.V., Ed., Vladivostok: Dal’nauka, 2014, pp. 309–324.

    Google Scholar 

  5. Selina, M.S., Distribution of potentially toxic dinoflagellates Dinophysis (Dinophyta) in Vostok Bay, Sea of Japan, Russ. J. Mar. Biol., 1993, vol. 19, nos. 5–6, pp. 299–302.

    Google Scholar 

  6. Sychev, K.S., Prakticheskii kurs zhidkostnoi khromatografii (Practical Course on Liquid Chromatography), Moscow: KOKORO, 2013.

    Google Scholar 

  7. Tekhnicheskii Reglament Tamozhennogo Soyuza TRTS 021/2011 “O bezopasnosti pishchevoi produktsii”: utv. resheniem Komissii Tamozhennogo Soyuza ot 9.12.2011 g. N 880 (Technical Regulations of the Customs Union TRTS 021/2011 “On Safety of Food Products”, Approved by Decision of the Customs Union Commission, December 9, 2011, no. 880).

  8. Metodicheskiye rekomendatsii MR01.016-07: “Ekspress-opredeleniye okadaikovoi kisloty v mollyuskakh s pomoshch’yu test-sistemy DSP-Check proizvodstva firmy Parapharm Laboratories Co., Ltd, Yaponiya” (Methodical Recommendations MR01.016-07: “Rapid Detection of Okadaic Acid in Shellfish Using the Test System DSP-Check Manufactured by Parapharm Laboratories, Japan”), Moscow: Rospotrebnadzor, 2007.

  9. Blanco, J., Marino, C., Martin, H., et al., Anatomical distribution of diarrhetic shellfish poisoning (DSP) toxins in the mussel Mytilus galloprovincialis, Toxicon, 2007, vol. 50, no. 8, pp. 1011–1018.

    Article  CAS  PubMed  Google Scholar 

  10. Carmody, P., James, J.K., and Kelly, S.S., Dinophysistoxin- 2: the predominant diarrhetic shellfish toxin in Ireland, Toxicon, 1996, vol. 34, no. 3, pp. 351–359.

    Article  CAS  PubMed  Google Scholar 

  11. Garcia, C., Truan, D., Lagos, M., et al., Metabolic transformation of dinophysistoxin-3 into dinophysistoxin- 1 causes human intoxication by consumption of O-acyl-derivatives dinophysistoxins contaminated shellfish, J. Toxicol. Sci., 2005, vol. 30, no. 4, pp. 287–296.

    Article  CAS  PubMed  Google Scholar 

  12. Hammert, C., Lucas, B., and Kirschbaum, J., HPLC/MS determination of diarrhetic shellfish poisoning (DSP) toxins as 4-bromomethyl-7-methoxycoumarin derivatives, in Harmful Marine Algal Blooms, Paris: Lavoisier, 1995, pp. 297–302.

    Google Scholar 

  13. Hoppenrath, M., Chomerat, N., Horiguchi, T., et al., Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae)—a proposal and review, Harmful Algae, 2013, vol. 27, pp. 1–28.

    Article  Google Scholar 

  14. Imbs, A.B., Vologodskaya, A.V., Nevshupova, N.V., et al., Response of prostaglandin content in the red alga Gracilaria verrucosa to season and solar irradiance, Phytochemistry, 2001, vol. 58, no. 7, pp. 1067–1072.

    Article  CAS  PubMed  Google Scholar 

  15. Kameneva, P.A., Efimova, K.V., Rybin, V.G., et al., Detection of dinophysistoxin-1 in clonal culture of marine dinoflagellate Prorocentrum foraminosum (Faust M.A., 1993) from the Sea of Japan, Toxins, 2015, vol. 7, no. 10, pp. 3947–3959.

    CAS  Google Scholar 

  16. Kameneva, P.A., Imbs, A.B., and Orlova, T.Yu., Distribution of DTX-3 in edible and non-edible parts of Crenomytilus grayanus from the Sea of Japan, Toxicon, 2015, vol. 93, pp. 1–3.

    Article  Google Scholar 

  17. Lee, J.S., Igarashi, T., Fraga, S., et al., Determination of diarrhetic shellfish toxins in various dinoflagellate species, J. Appl. Phycol., 1989, vol. 1, no. 2, pp. 147–152.

    Article  Google Scholar 

  18. Lee, J.S., Yanagi T., Kenma, R., et al., Fluorometric determination of diarrhetic shellfish poisoning by high performance liquid chromatography, Agric. Biol. Chem., 1987, vol. 51, no. 3, pp. 877–881.

    CAS  Google Scholar 

  19. Leftley, J. and Hannah, F., Phycotoxins in seafood, in Bioactive Compounds in Foods, London: Wiley, 2008, pp. 52–108.

    Chapter  Google Scholar 

  20. Luckas, B., Hummert, C., Thielert, G., et al., Improvement of HPLC/fluorescence and HPLC/MS procedures for the determination of DSP and PSP toxins in contaminated shellfish, in EUR Report No. 15339, Luxembourg: Eur. Comm., 1994.

    Google Scholar 

  21. Marr, J.C., McDowell, L.M., and Quilliam, M.A., Investigation of derivatization reagents for the analysis of diarrhetic shellfish poisoning toxins by liquid chromatography with fluorescence detection, Nat. Toxins, 1994, vol. 2, no. 5, pp. 302–311.

    Article  CAS  PubMed  Google Scholar 

  22. McNabb, P., Chemistry, metabolism and chemical analysis of okadaic acid group toxins, in Seafood and Freshwater Toxins: Pharmacology, Physiology and Detection, Boca Raton: CRC, 2008, pp. 209–228.

    Chapter  Google Scholar 

  23. Morton, S., Vershinin, A., Laurinda, L.S., et al., Seasonality of Dinophysis spp. and Prorocentrum lima in Black Sea phytoplankton and associated shellfish toxicity, Harmful Algae, 2009, vol. 8, no. 5, pp. 629–636.

    Article  Google Scholar 

  24. Orlova, T.Yu., Toxic microalgae in plankton, benthic and epiphytic assemblages from the north-western Sea of Japan, Proc. 9th IST Asia Pacific Meeting “Animal, Plant and Microbial Toxins,” Vladivostok, Russia, September 4–8, 2011, Vladivostok: Dal’nauka, 2011, p. 40.

    Google Scholar 

  25. Orlova, T.Yu., Kameneva, P.A., Stonik, I.V., et al., Diarrhetic shellfish toxins in Primorsky krai, Russia, J. Shellfish Res., 2015, vol. 34, no. 3, pp. 1151–1160.

    Article  Google Scholar 

  26. Reguera, B., Velo-Suarez, L., Raine, R., et al., Harmful Dinophysis species: a review, Harmful Algae, 2012, vol. 14, pp. 87–106.

    Article  Google Scholar 

  27. Stabell, O.B., Hormazabal, V., Steffenak, I., et al., Diarrhetic shellfish toxins: improvement of sample clean-up for HPLC determination, Toxicon, 1991, vol. 29, no. 1, pp. 21–29.

    Article  CAS  PubMed  Google Scholar 

  28. Suzuki, T., Ota, H., and Yamasaki, M., Direct evidence of transformation of dinophysistoxin-1 to 7-O-acyldinophysistoxin- 1 (dinophysistoxin-3) in the scallop Patinopecten yessoensis, Toxicon, 1999, vol. 37, no. 1, pp. 187–198.

    Article  CAS  PubMed  Google Scholar 

  29. Takai, A., Murata, M., Torigoe, K., et al., Inhibitory effect of okadaic acid derivatives on protein phosphatases, Biochem. J., 1992, vol. 284, no. 2, pp. 539–544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Valdiglesias, V., Prego-Faraldo, M.V., Pasaro, E., et al., Okadaic acid: more than a diarrheic toxin, Mar. Drugs, 2013, vol. 11, no. 11, pp. 4328–4349.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Vale, P. and Sampayo, M.A., Esterification of DSP toxins by Portuguese bivalves from the northwest coast determined by LC-MS—a widespread phenomenon, Toxicon, 2002, vol. 40, no. 1, pp. 33–42.

    Article  CAS  PubMed  Google Scholar 

  32. Vershinin, A., Moruchkov, A., Morton, S., et al., Phytoplankton composition of the Kandalaksha Gulf, Russian White Sea: Dinophysis and lipophilic toxins in the blue mussel (Mytilus edulis), Harmful Algae, 2006, vol. 5, no. 5, pp. 558–564.

    Google Scholar 

  33. Yanagi, T., Murata, M., Torigoe, K., et al., Biological activities of semisynthetic analogs of DTX-3 and major diarrhetic shellfish toxins, Agric. Biol. Chem., 1989, vol. 53, no. 2, pp. 525–529.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. A. Kameneva.

Additional information

Original Russian Text © P.A. Kameneva, T.Yu. Orlova, A.B. Imbs, 2016, published in Biologiya Morya.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kameneva, P.A., Orlova, T.Y. & Imbs, A.B. The seasonal dynamics of diarrhetic shellfish poisoning toxins in the digestive gland of Crenomytilus grayanus (Dunker, 1853) analyzed by high-performance liquid chromatography with fluorometric detection. Russ J Mar Biol 42, 258–265 (2016). https://doi.org/10.1134/S1063074016030056

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1063074016030056

Keywords

Navigation