Brazilian Journal of Botany

, Volume 41, Issue 1, pp 209–218 | Cite as

First detection of species of the potentially toxic genus Azadinium (Amphidomataceae, Dinophyceae) in tropical coastal waters of Brazil

  • Kaoli Pereira Cavalcante
  • Sylvia Maria Moreira Susini-Ribeiro
  • Urban Tillmann
Original Article
  • 37 Downloads

Abstract

In fall 1995, during a survey in Abrolhos coral reef system (southwestern Atlantic, Brazil), significant densities (143–6174 cells L−1) of small thecate dinoflagellates were detected. Analysis of this material in scanning and transmission electron microscopy confirmed the presence of four taxa assigned to the potentially toxic genus Azadinium: A. dexteroporum Percopo et Zingone, A. luciferelloides Tillmann et Akselman, A. cf. polongum Tillmann and Azadinium sp. The latter taxon showed external morphological features quite distinct from any Azadinium taxon yet described, but its formal description as a new species depends on more detailed analysis. Species of Azadinium have never been confirmed in Brazilian waters until now, although the toxins produced by these dinoflagellates, the azaspiracids, have been detected in Brazilian southern coast without recognition of their producing organisms. The highest densities of Azadinium spp. occurred at stations south of and over the Abrolhos Bank, which receive higher nutrient concentrations due to upwelling of deep and nutrient-rich water masses.

Keywords

Dinophyta Electron microscopy Harmful algae Nanoplankton South America 

Notes

Acknowledgements

The JOPS-II Project was financed by the Ministries of Science and Technology of Brazil (MCT and MMA/IBAMA) and Germany (BMBF, Project No. 03f0144A). Sylvia Maria Moreira Susini-Ribeiro was supported by FAPESP (No. 93/2907-8) and CNPq Research grant. Special thanks are given to Drs. Salvador Airton Gaeta and Mayza Pompeu for providing all oceanographic datasets used in this paper.

References

  1. Akselman R, Negri RM (2012) Blooms of Azadinium cf. spinosum Elbrächter et Tillmann (Dinophyceae) in northern shelf waters of Argentina, Southwestern Atlantic. Harmful Algae 19:30–38.  https://doi.org/10.1016/j.hal.2012.05.004 CrossRefGoogle Scholar
  2. Álvarez G, Uribe E, Ávalos P, Mariño C, Blanco J (2010) First identification of azaspiracid and spirolides in Mesodesma donacium and Mulinia edulis from Northern Chile. Toxicon 55:638–641.  https://doi.org/10.1016/j.toxicon.2009.07.014 CrossRefPubMedGoogle Scholar
  3. Amzil Z, Sibat M, Royer F, Savar V (2008) First report on azaspiracid and yessotoxin groups detection in French shellfish. Toxicon 52:39–48.  https://doi.org/10.1016/j.toxicon.2008.05.006 CrossRefPubMedGoogle Scholar
  4. Bacchiocchi S, Siracusa M, Ruzzi A, Gorbi S, Ercolessi M, Cosentino MA, Ammazzalorso P, Orletti R (2015) Two-year study of lipophilic marine toxin profile in mussels of the North-central Adriatic Sea: first report of azaspiracids in Mediterranean seafood. Toxicon 108:115–125.  https://doi.org/10.1016/j.toxicon.2015.10.002 CrossRefPubMedGoogle Scholar
  5. Braña Magdalena A, Lehane M, Krys S, Fernández ML, Furey A, James KJ (2003) The first identification of azaspiracids in shellfish from France and Spain. Toxicon 42:105–108.  https://doi.org/10.1016/S0041-0101(03)00105-3 CrossRefGoogle Scholar
  6. Colman JR, Twiner MJ, Hess P, McMahon P, Satake M, Yasumoto T, Doucette GJ, Ramsdell SJ (2005) Teratogenic effects of azaspiracid-1 identified by microinjection of Japanese medaka (Oryzias latipes) embryos. Toxicon 45:881–890.  https://doi.org/10.1016/j.toxicon.2005.02.014 CrossRefPubMedGoogle Scholar
  7. Ekau W, Knoppers B (1999) An introduction to the pelagic system of the North-East and East Brazilian shelf. Arch Fish Mar Res 47:113–119Google Scholar
  8. Elgarch A, Vale P, Rifai S, Fassouane A (2008) Detection of diarrheic shellfish poisoning and azaspiracid toxins in Moroccan mussels: comparison of the LC-MS method with the commercial immunoassay kit. Mar Drugs 6:587–594.  https://doi.org/10.3390/md6040587 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Furey A, O’Doherty S, O’Callaghan K, Lehane M, James KJ (2010) Azaspiracid poisoning (AZP) toxins in shellfish: toxicological and health considerations. Toxicon 56:173–190.  https://doi.org/10.1016/j.toxicon.2009.09.009 CrossRefPubMedGoogle Scholar
  10. Gaeta SA, Lorenzzetti JA, Miranda LB, Susini-Ribeiro SMM, Pompeu M, Araujo CES (1999) The Vitória Eddy and its relation to the phytoplankton biomass and primary productivity during the austral fall of 1995. Arch Fish Mar Res 47:253–270Google Scholar
  11. Grasshoff K (1983) Methods for seawater analysis. Weissheim Verlag Chemie, New YorkGoogle Scholar
  12. Hess P, McCarron P, Krock B, Kilcoyne J, Miles CO (2014) Azaspiracids: chemistry, biosynthesis, metabolism, and detection. In: Botana LM (ed) Seafood and freshwater toxins: phamacology, physiology, and detection. CRC Press, Boca Raton, pp 799–821CrossRefGoogle Scholar
  13. Ito E, Satake M, Ofuji K, Higashi M, Harigaya K, McMahon T, Yasumoto T (2002) Chronic effects in mice caused by oral administration of sublethal doses of azaspiracid, a new marine toxin isolated from mussels. Toxicon 40:193–203.  https://doi.org/10.1016/S0041-0101(01)00226-4 CrossRefPubMedGoogle Scholar
  14. James KJ, Furey A, Lehane M, Ramstad H, Aune T, Hovgaard P, Morris S, Higman W, Satake M, Yasumoto T (2002) First evidence of an extensive northern European distribution of azaspiracid poisoning (AZP) toxins in shellfish. Toxicon 40:909–915.  https://doi.org/10.1016/S0041-0101(02)00082-X CrossRefPubMedGoogle Scholar
  15. Krock B, Tillmann U, Voß D, Koch BP, Salas R, Witt M, Potvin E, Jeong HJ (2012) New azaspiracids in Amphidomataceae (Dinophyceae). Toxicon 60:830–839.  https://doi.org/10.1016/j.toxicon.2012.05.007 CrossRefPubMedGoogle Scholar
  16. Krock B, Tillmann U, Alpermann TJ, Voß D, Zielinski O, Cembella AD (2013) Phycotoxin composition and distribution in plankton fractions from the German Bight and western Danish coast. J Plankton Res 35:1093–1108.  https://doi.org/10.1093/plankt/fbt054 CrossRefGoogle Scholar
  17. Krock B, Tillmann U, Witt M, Gu H (2014) Azaspiracid variability of Azadinium poporum (Dinophyceae) from the China Sea. Harmful Algae 36:22–28.  https://doi.org/10.1016/j.hal.2014.04.012 CrossRefGoogle Scholar
  18. Luo Z, Gu H, Krock B, Tillmann U (2013) Azadinium dalianense, a new dinoflagellate species from the Yellow Sea, China. Phycologia 52:625–636.  https://doi.org/10.2216/13-178.1 CrossRefGoogle Scholar
  19. Luo Z, Krock B, Mertens KN, Nézan E, Chomérat N, Bilien G, Tillmann U, Gu H (2017) Adding new pieces to the Azadinium (Dinophyceae) diversity and biogeography puzzle: non-toxigenic Azadinium zhuanum sp. nov. from China, toxigenic A. poporum from the Mediterranean, and a non-toxigenic A. dalianense from the French Atlantic. Harmful Algae 66:65–78.  https://doi.org/10.1016/j.hal.2017.05.001 CrossRefPubMedGoogle Scholar
  20. Massucatto A, Pilotto ALS, Schramm MA (2014) Investigação da presença de azaspirácidos em recursos pesqueiros do Canal do Linguado. In: Resumos do 4º Seminário de Pesquisa, Extensão e Inovação do Instituto Federal de Santa Catarina. IFSC, Florianópolis, pp 1–3Google Scholar
  21. McMahon T, Silke J (1996) West coast of Ireland; winter toxicity of unknown aetiology in mussels. Harmful Algae News 14:2Google Scholar
  22. Nézan E, Tillmann U, Bilien G, Boulben S, Chèze K, Zentz F, Salas R, Chomérat N (2012) Taxonomic revision of the dinoflagellate Amphidoma caudata: transfer to the genus Azadinium (Dinophyceae) and proposal of two varieties, based on morphological and molecular phylogenetic analyses. J Phycol 48:925–939.  https://doi.org/10.1111/j.1529-8817.2012.01159.x CrossRefPubMedGoogle Scholar
  23. Percopo I, Siano R, Rossi R, Soprano V, Sarno D, Zingone A (2013) A new potentially toxic Azadinium species (Dinophyceae) from the Mediterranean Sea. A. dexteroporum sp. nov. J Phycol 49:950–966.  https://doi.org/10.1111/jpy.12104 PubMedGoogle Scholar
  24. Pereira AF, Belém AL, Castro BM, Geremias R (2005) Tide-topography interaction along the eastern Brazilian shelf. Cont Shelf Res 25:1521–1539.  https://doi.org/10.1016/j.csr.2005.04.008 CrossRefGoogle Scholar
  25. Proença LAO, Schramm MA, Santos KRS, Martins H, Alves TP, Menezes M (2014) Azaspiracid production by an Azadinium like flagellate isolated from a shallow mixosohaline mangrove system at southern Brazilian coast. In: Proceedings of 16th international conference on harmful algae. ISSHA, Wellington, p 121Google Scholar
  26. Rossi R, Dell’aversano C, Krock B, Ciminiello P, Percopo I, Tillmann U, Soprano V, Zingone A (2017) Mediterranean Azadinium dexteroporum (Dinophyceae) produces AZA-35 and six novel azaspiracids: a structural study by a multi-platform mass spectrometry approach. Anal Bioanal Chem 409:1121–1134.  https://doi.org/10.1007/s00216-016-0037-4 CrossRefPubMedGoogle Scholar
  27. Satake M, Ofuji K, Naoki H, James KJ, Furey A, McMahon T, Silke J, Yasumoto T (1998) Azaspiracid, a new marine toxin having unique spiro ring assemblies, isolated from irish mussels, Mytilus edulis. J Am Chem Soc 120:9967–9968.  https://doi.org/10.1021/ja981413r CrossRefGoogle Scholar
  28. Schramm MA, Alves TP, Honorato MC, Proença LAO (2010) Primeira detecção de ficotoxinas lipofílicas em mexilhões da Armação do Itapocorói em Santa Catarina através de LC-MS/MS. In: Anais do XIII Congresso Brasileiro de Ficologia. Sociedade Brasileira de Ficologia, Paraty, p 381Google Scholar
  29. Susini-Ribeiro SMM (1996) Caracterização taxonômica e ecológica das comunidades pico-, nano- e microplanctônicas, superficial e profunda, da zona eufótica do Atlântico Sul. Ph.D. thesis, Universidade de São Paulo, São PauloGoogle Scholar
  30. Susini-Ribeiro SMM (1999) Biomass distribution of pico-, nano- and microplankton on the continental shelf of Abrolhos, East Brazil. Arch Fish Mar Res 47:271–284Google Scholar
  31. Susini-Ribeiro SMM, Pompeu M, Gaeta SA, Souza JSD, Masuda LSD (2013) Topographical and hydrological impacts on the structure of microphytoplankton assemblages on the Abrolhos Bank region, Brazil. Cont Shelf Res 70:88–96.  https://doi.org/10.1016/J.csr.2013.09.023 CrossRefGoogle Scholar
  32. Taleb H, Vale P, Amanhir R, Benhadouch A, Sagou R, Chafik A (2006) First detection of azaspiracids in mussels in north west Africa. J Res 25:1067–1070.  https://doi.org/10.2983/0730-8000(2006)25[1067:FDOAIM]2.0.CO;2 Google Scholar
  33. Tillmann U, Akselman R (2016) Revisiting the 1991 algal bloom in shelf waters off Argentina: Azadinium luciferelloides sp. nov. (Amphidomataceae, Dinophyceae) as the causative species in a diverse community of other amphidomataceans. Phycol Res 64:160–175.  https://doi.org/10.1111/pre.12133 CrossRefGoogle Scholar
  34. Tillmann U, Elbrächter M, Krock B, John U, Cembella A (2009) Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. Eur J Phycol 44:63–79.  https://doi.org/10.1080/09670260802578534 CrossRefGoogle Scholar
  35. Tillmann U, Elbrächter M, John U, Krock B, Cembella A (2010) Azadinium obesum (Dinophyceae), a new nontoxic species in the genus that can produce azaspiracid toxins. Phycologia 49:169–182.  https://doi.org/10.2216/PH09-35.1 CrossRefGoogle Scholar
  36. Tillmann U, Elbrächter M, John U, Krock B (2011) A new non-toxic species in the dinoflagellate genus Azadinium: A. poporum sp. nov. Eur J Phycol 46:74–87.  https://doi.org/10.1080/09670262.2011.556753 CrossRefGoogle Scholar
  37. Tillmann U, Söhner S, Nézan E, Krock B (2012) First record of Azadinium from the Shetland Islands including the description of A. polongum sp. nov. Harmful Algae 20:142–155.  https://doi.org/10.1016/j.hal.2012.10.001 CrossRefGoogle Scholar
  38. Tillmann U, Gottschling M, Nézan E, Krock B, Bilien G (2014a) Morphological and molecular characterization of three new Azadinium species (Amphidomataceae, Dinophyceae) from the Irminger Sea. Protist 165:417–444.  https://doi.org/10.1016/j.protis.2014.04.004 CrossRefPubMedGoogle Scholar
  39. Tillmann U, Salas R, Jauffrais T, Hess P, Silke J (2014b) AZA: the producing organisms—biology and trophic transfer. In: Botana LM (ed) Seafood and freshwater toxins. CRC Press, Boca Raton, pp 773–798CrossRefGoogle Scholar
  40. Tillmann U, Gottschling M, Nézan E, Krock B (2015) First record of Azadinium dexteroporum and Amphidoma languida (Amphidomataceae, Dinophyceae) from the Irminger Sea off Iceland. Mar Biodivers Rec 8:1–11.  https://doi.org/10.1017/S1755267215001128 CrossRefGoogle Scholar
  41. Tillmann U, Borel CM, Barrera F, Lara R, Krock B, Almandoz GO, Witt M, Trefault N (2016) Azadinium poporum from the Argentine Continental Shelf, Southwestern Atlantic, produces azaspiracid-2 and azaspiracid-2 phosphate. Harmful Algae 51:40–55.  https://doi.org/10.1016/j.hal.2015.11.001 CrossRefPubMedGoogle Scholar
  42. Tillmann U, Jaén D, Fernández L, Gottschling M, Witt M, Blanco J, Krock B (2017a) Amphidoma languida (Amphidomatacea, Dinophyceae) with a novel azaspiracid toxin profile identified as the cause of molluscan contamination at the Atlantic coast of southern Spain. Harmful Algae 62:113–126.  https://doi.org/10.1016/j.hal.2016.12.001 CrossRefPubMedGoogle Scholar
  43. Tillmann U, Trefault N, Krock B, Parada-Pozo G, De La Iglesia R, Vásquez M (2017b) Identification of Azadinium poporum (Dinophyceae) in the Southeast Pacific: morphology, molecular phylogeny, and azaspiracid profile characterization. J Plankton Res 39:350–367.  https://doi.org/10.1093/plankt/fbw099 Google Scholar
  44. Tillmann U, Sánchez-Ramires S, Krock B, Bernales-Jiménez A (in revision) A bloom of Azadinium polongum (Dinophyceae) in coastal waters off Peru. In revision, Revista de Biología Marina y OceanografíaGoogle Scholar
  45. Trainer VL, Moore L, Bill BD, Adams NG, Harrington N, Borchert J, Silva DAM, Eberhard BTL (2013) Diarrhetic shellfish toxins and other lipophilic toxins of human health concern in Washington State. Mar Drugs 11:1815–1835.  https://doi.org/10.3390/md11061815 CrossRefPubMedCentralPubMedGoogle Scholar
  46. Turner AD, Goya AB (2015) Occurrence and profiles of lipophilic toxins in shellfish harvested from Argentina. Toxicon 102:32–42.  https://doi.org/10.1016/j.toxicon.2015.05.010 CrossRefPubMedGoogle Scholar
  47. Twiner M, Hess P, Doucette GJ (2014) Azaspiracids: toxicology, pharmacology, and risk assessment. In: Botana LM (ed) Seafood and freshwater toxins. CRC Press, Boca Raton, pp 823–855CrossRefGoogle Scholar
  48. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton: Methodik. Mitt Int Ver Theor Angew Limnol 9:1–39Google Scholar
  49. Vale P, Bire R, Hess P (2008) Confirmation by LC–MS/MS of azaspiracids in shellfish from the Portuguese north-western coast. Toxicon 51:1449–1456.  https://doi.org/10.1016/j.toxicon.2008.03.022 CrossRefPubMedGoogle Scholar
  50. Yao J, Tan Z, Zhou D, Guo M, Xing L, Yang S (2010) Determination of azaspiracid-1 in shellfishes by liquid chromatography with tandem mass spectrometry. Chin J Chromatogr 28:363–367.  https://doi.org/10.3724/SP.J.1123.2010.00363 CrossRefGoogle Scholar
  51. Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Res 10:221–231.  https://doi.org/10.1016/0011-7471(63)90358-9 Google Scholar

Copyright information

© Botanical Society of Sao Paulo 2018

Authors and Affiliations

  • Kaoli Pereira Cavalcante
    • 1
  • Sylvia Maria Moreira Susini-Ribeiro
    • 1
  • Urban Tillmann
    • 2
  1. 1.Universidade Estadual de Santa CruzIlhéusBrazil
  2. 2.Alfred Wegener Institute Helmholtz Centre for Polar- and Marine ResearchBremerhavenGermany

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