Production and isolation of azaspiracid-1 and -2 from Azadinium spinosum culture in pilot scale photobioreactors

Marine Drugs

Volumn 10, Issue 6, 2012, Pages 1360-1382

  Jauffrais, Thierry ^a   Kilcoyne, Jane ^b   Séchet, Véronique ^a   Herrenknecht, Christine ^c   Truquet, Philippe ^a   Hervé, Fabienne ^a   Bérard, Jean Baptiste ^a   Nulty, Cíara ^b   Taylor, Sarah ^a   Tillmann, Urban ^c   Miles, Christopher O ^d   Hess, Philipp ^a  

^a IFREMER   (France)

^b MARINE INSTITUTE   (Ireland)

^c UNIVERSITÉ DE NANTES   (France)

^d NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

Azaspiracid; Chemostat; Dinoflagellate; HP 20; LC MS MS; Micro algae; Photobioreactor; Solid phase extraction; Tangential flow filtration

Indexed keywords

AZASPIRACID; AZASPIRACID 1; AZASPIRACID 2; UNCLASSIFIED DRUG;

ALGA; ARTICLE; AZADINIUM SPINOSUM; CELL COUNT; CELL SUSPENSION; CENTRIFUGATION; CONTROLLED STUDY; DINOFLAGELLATE; NONHUMAN; PHOTOBIOREACTOR; PILOT STUDY; PROCESS OPTIMIZATION; SOLID PHASE EXTRACTION; STEADY STATE; TOXIN ANALYSIS; TOXIN STRUCTURE; TOXIN SYNTHESIS;

ALGAE; DINOPHYCEAE;

EID: 84863486845     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md10061360     Document Type: Article

References (61)

1. McMahon, T.; Silke, J. West coast of Ireland winter toxicity of unknown aetiology in mussels. Harmful Algae News 1996, 14, 2.
2. Satake, M.; Ofuji, K.; Naoki, H.; James, K.J.; Furey, A.; McMahon, T.; Silke, J.; Yasumoto, T. Azaspiracid, a new marine toxin having unique spiro ring assemblies, isolated from Irish mussels, Mytilus edulis. J. Am. Chem. Soc. 1998, 120, 9967-9968. (Pubitemid 28462514)
3. Nicolaou, K.C.; Koftis, T.V.; Vyskocil, S.; Petrovic, G.; Tang, W.J.; Frederick, M.O.; Chen, D.Y.K.; Li, Y.W.; Ling, T.T.; Yamada, Y.M.A. Total synthesis and structural elucidation of azaspiracid-1. Final assignment and total synthesis of the correct structure of azaspiracid-1. J. Am. Chem. Soc. 2006, 128, 2859-2872.
4. Ofuji, K.; Satake, M.; McMahon, T.; Silke, J.; James, K.J.; Naoki, H.; Oshima, Y.; Yasumoto, T. Two analogs of azaspiracid isolated from mussels, Mytilus edulis, involved in human intoxication in Ireland. Nat. Toxins 1999, 7, 99-102.
5. Ofuji, K.; Satake, M.; McMahon, T.; James, K.J.; Naoki, H.; Oshima, Y.; Yasumoto, T. Structures of azaspiracid analogs, azaspiracid-4 and azaspiracid-5, causative toxins of azaspiracid poisoning in Europe. Biosci. Biotechnol. Biochem. 2001, 65, 740-742. (Pubitemid 33615955)
6. Diaz Sierra, M.; Furey, A.; Hamilton, B.; Lehane, M.; James, K.J. Elucidation of the fragmentation pathways of azaspiracids, using electrospray ionisation, hydrogen/deuterium exchange, and multiple-stage mass spectrometry. J. Mass Spectrom. 2003, 38, 1178-1186. (Pubitemid 37508685)
7. James, K.J.; Sierra, M.D.; Lehane, M.; Magdalena, A.B.; Furey, A. Detection of five new hydroxyl analogues of azaspiracids in shellfish using multiple tandem mass spectrometry. Toxicon 2003, 41
8. Rehmann, N.; Hess, P.; Quilliam, M.A. Discovery of new analogs of the marine biotoxin azaspiracid in blue mussels (Mytilus edulis) by ultra-performance liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2008, 22, 549-558. (Pubitemid 351300590)
9. McCarron, P.; Kilcoyne, J.; Miles, C.O.; Hess, P. Formation of azaspiracids-3, -4, -6, and -9 via decarboxylation of carboxyazaspiracid metabolites from shellfish. J. Agric. Food. Chem. 2009, 57, 160-169.
10. Krock, B.; Tillmann, U.; John, U.; Cembella, A. LC-MS-MS aboard ship: tandem mass spectrometry in the search for phycotoxins and novel toxigenic plankton from the North Sea. Anal. Bioanal. Chem. 2008, 392, 797-803.
11. Krock, B.; Tillmann, U.; John, U.; Cembella, A.D. Characterization of azaspiracids in plankton size-fractions and isolation of an azaspiracid- producing dinoflagellate from the North Sea. Harmful Algae 2009, 8, 254-263.
12. Tillmann, U.; Elbrachter, M.; Krock, B.; John, U.; Cembella, A. Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. Eur. J. Phycol. 2009, 44, 63-79.
13. Salas, R.; Tillmann, U.; John, U.; Kilcoyne, J.; Burson, A.; Cantwell, C.; Hess, P.; Jauffrais, T.; Silke, J. The role of Azadinium spinosum (Dinophyceae) in the production of azaspiracid shellfish poisoning in mussels. Harmful Algae 2011, 10, 774-783.
14. Hernandez-Becerril, D.U.; Escobae-Morales, S.; Morreno-Gutiérez, S.P.; Baron-Campis, S.A. Two new Records of Potentially toxic Phytoplankton Species from the Mexican Pacific. In Abstract Book of the 14th International Conference Harmful Algae; Hellenic Centre for Marine Research: Hersonissos, Greece, 2010; p. 137.
15. Akselman, R.; Negri, R.M. Azadinium spinosum Elbrächter et Tillmann (Dinophyceae) is Present and also caused Blooms at the Southwestern Atlantic. In Abstract Book of the 14th International Conference Harmful Algae; Hellenic Centre for Marine Research: Hersonissos, Greece, 2010; p. 132.
16. Potvin, E.; Jeong, H.J.; Kang, N.S.; Tillmann, U.; Krock, B. First report of the photosynthetic dinoflagellate genus Azadinium in the Pacific Ocean: Morphology and molecular characterization of Azadinium cf. poporum. J. Eukaryot. Microbiol. 2012, 59, 145-156.
17. Amzil, Z.; Sibat, M.; Royer, F.; Savar, V. First report on azaspiracid and yessotoxin groups detection in French shellfish. Toxicon 2008, 52, 39-48.
18. Vale, P.; Bire, R.; Hess, P. Confirmation by LC-MS/MS of azaspiracids in shellfish from the Portuguese north-western coast. Toxicon 2008, 51, 1449-1456.
19. Taleb, H.; Vale, P.; Amanhir, R.; Benhadouch, A.; Sagou, R.; Chafik, A. First detection of azaspiracids in mussels in north west Africa. J. Shellfish Res. 2006, 25, 1067-1070. (Pubitemid 46025294)
20. James, K.J.; Furey, A.; Lehane, M.; Ramstad, H.; Aune, T.; Hovgaard, P.; Morris, S.; Higman, W.; Satake, M.; Yasumoto, T. First evidence of an extensive northern European distribution of azaspiracid poisoning (AZP) toxins in shellfish. Toxicon 2002, 40, 909-915. (Pubitemid 34663683)
21. Ueoka, R.; Ito, A.; Izumikawa, M.; Maeda, S.; Takagi, M.; Shin-Ya, K.; Yoshida, M.; van Soest, R.W.M.; Matsunaga, S. Isolation of azaspiracid-2 from a marine sponge Echinoclathria sp. as a potent cytotoxin. Toxicon 2009, 53,
22. Alvarez, G.; Uribe, E.; Avalos, P.; Marino, C.; Blanco, J. First identification of azaspiracid and spirolides in Mesodesma donacium and Mulinia edulis from Northern Chile. Toxicon 2010, 55, 638-641.
23. Twiner, M.J.; Rehmann, N.; Hess, P.; Doucette, G.J. Azaspiracid shellfish poisoning: A review on the chemistry, ecology, and toxicology with an emphasis on human health impacts. Mar. Drugs 2008, 6, 39-72. (Pubitemid 351919074)
24. Tillmann, U.; Elbrachter, M.; John, U.; Krock, B.; Cembella, A. Azadinium obesum (Dinophyceae), a new nontoxic species in the genus that can produce azaspiracid toxins. Phycologia 2010, 49, 169-182.
25. Tillmann, U.; Elbrachter, M.; John, U.; Krock, B. A new non-toxic species in the dinoflagellate genus Azadinium: A. poporum sp. nov. Eur. J. Phycol. 2011, 46, 74-87.
26. Krock, B.; Tillmann, U.; Voß, D.; Koch, B.P.; Salas, R.; Witt, M.; Potvin, É.; Jeong, H.J. New azaspiracids in Amphidomataceae (Dinophyceae). Toxicon 2012, doi:10.1016/j.toxicon.2012.05.007.
27. 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.
28. Abraham, A.; Plakas, S.M.; Wang, Z.H.; Jester, E.L.E.; El Said, K.R.; Granade, H.R.; Henry, M.S.; Blum, P.C.; Pierce, R.H.; Dickey, R.W. Characterization of polar brevetoxin derivatives isolated from Karenia brevis cultures and natural blooms. Toxicon 2006, 48, 104-115. (Pubitemid 44137269)
29. Laycock, M.V.; Thibault, P.; Ayer, S.W.; Walter, J.A. Isolation and purification procedures for the preparation of paralytic shellfish poisoning toxin standards. Nat. Toxins 1994, 2, 175-183. (Pubitemid 24222681)
30. Loader, J.I.; Hawkes, A.D.; Beuzenberg, V.; Jensen, D.J.; Cooney, J.M.; Wilkins, A.L.; Fitzgerald, J.M.; Briggs, L.R.; Miles, C.O. Convenient large-scale purification of yessotoxin from Protoceratium reticulatum culture and isolation of a novel furanoyessotoxin. J. Agric. Food. Chem. 2007, 55, 11093-11100.
31. Torigoe, K.; Murata, M.; Yasumoto, T.; Iwashita, T. Prorocentrolide, a toxic nitrogeneous macrocycle from a marine dinoflagellate. Prorocentrum lima. J. Am. Chem. Soc. 1988, 110, 7876-7877.
32. Miles, C.O.; Wilkins, A.L.; Stirling, D.J.; MacKenzie, A.L. Gymnodimine C, an isomer of gymnodimine B, from Karenia selliformis . J. Agric. Food. Chem. 2003, 51, 4838-4840.
33. Selwood, A.I.; Miles, C.O.; Wilkins, A.L.; van Ginkel, R.; Munday, R.; Rise, F.; McNabb, P. Isolation, structural determination and acute toxicity of pinnatoxins E, F and G. J. Agric. Food. Chem. 2010, 58, 6532-6542.
34. Miles, C.O.; Wilkins, A.L.; Munday, R.; Dines, M.H.; Hawkes, A.D.; Briggs, L.R.; Sandvik, M.; Jensen, D.J.; Cooney, J.M.; Holland, P.T.; et al. Isolation of pectenotoxin-2 from Dinophysis acuta and its conversion to pectenotoxin-2 seco acid, and preliminary assessment of their acute toxicities. Toxicon 2004, 43, 1-9.
35. Perez, R.A.; Rehmann, N.; Crain, S.; LeBlanc, P.; Craft, C.; MacKinnon, S.; Reeves, K.; Burton, I.W.; Walter, J.A.; Hess, P.; et al. The preparation of certified calibration solutions for azaspiracid-1,-2, and-3, potent marine biotoxins found in shellfish. Anal. Bioanal. Chem. 2010, 398,
36. Kilcoyne, J.; Keogh, A.; Clancy, G.; Leblanc, P.; Burton, I.; Quilliam, M.A.; Hess, P.; Miles, C.O. Improved isolation procedure for azaspiracids from shellfish, structural elucidation of azaspiracid-6, and stability studies. J. Agric. Food. Chem. 2012, 60, 2447-2455.
37. Rundberget, T.; Sandvik, M.; Larsen, K.; Pizarro, G.M.; Reguera, B.; Castberg, T.; Gustad, E.; Loader, J.I.; Rise, F.; Wilkins, A.L.; Miles, C.O. Extraction of microalgal toxins by large-scale pumping of seawater in Spain and Norway, and isolation of okadaic acid and dinophysistoxin-2. Toxicon 2007, 50, 960-970. (Pubitemid 350030929)
38. Hess, P.; McCarron, P.; Quilliam, M.A. Fit-for-purpose shellfish reference materials for internal and external quality control in the analysis of phycotoxins. Anal. Bioanal. Chem. 2007, 387, 2463-2474. (Pubitemid 46384963)
39. European Union. Commission Regulation (EU) No 15/2011 of 10 January 2011 Amending Regulation (EC) No 2074/2005 as Regards Recognised Testing Methods for Detecting Marine Biotoxins in Live Bivalve Molluscs; Off. J. Eur. Union L6, 11.1.2011; EU: Luxembourg, Luxembourg, 2011.
40. Séchet, V.; Berard, J.B.; Bohec, M.; Bougaran, G.; Carré, C.; Masselin, P.; Truquet, P. Growth and toxicity of Alexandrium catanella isolated from Thau Lagoon (France) Cultured in Stirred Tank Photobioreactors. In Proceeding of the 4th International Conference on Molluscan Shellfish Safety; Villalba, A., Reguera, B., Romalde, J.L., Beiras, R., Eds.; Intergovernmental Oceanographic Commision of UNESCO: Santiago de Compostella, Spain, 2003; pp. 135-144.
41. Séchet, V.; Berard, J.B.; Bohec, M.; Bougaran, G.; Carré, C.; Masselin, P.; Truquet, P. Continuous-Flow and batch Cultures of Toxic Alexandrium catanella and A. minutum in stirred Tank Bioreactors. In Proceeding of the 10th International Conference on Harmful Algae; Steidinger, K.A., Landsberg, J.H., Tomas, C.R., Vargo, G.A., Eds.; Florida Marine Research Institute, Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, Intergovernmental Oceanographic Commision of UNESCO: St. Pete Beach, FL, USA, 2004; pp. 399-401.
42. Gallardo Rodriguez, J.J.; Sanchez Miron, A.; Garcia Camacho, F.; Ceron Garcia, M.C.; Belarbi, E.H.; Chisti, Y.; Molina Grima, E. Causes of shear sensitivity of the toxic dinoflagellate Protoceratium reticulatum. Biotechnol. Prog. 2009, 25, 792-800.
43. Robinson, J.A. Polyketide synthase complexes: Their structure and function in antibiotic biosynthesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1991, 332, 107-114.
44. Schembri, M.A.; Neilan, B.A.; Saint, C.P. Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii . Environ. Toxicol. 2001, 16, 413-421. (Pubitemid 33040532)
45. Medhioub, W.; Sechet, V.; Truquet, P.; Bardouil, M.; Amzil, Z.; Lassus, P.; Soudant, P. Alexandrium ostenfeldii growth and spirolide production in batch culture and photobioreactor. Harmful Algae 2011, 10, 794-803.
46. Nagai, S.; Suzuki, T.; Nishikawa, T.; Kamiyama, T. Differences in the production and excretion kinetics of okadaic acid, dinophysistoxin-1, and pectenotoxin-2 between cultures of Dinophysis acuminata and Dinophysis fortii isolated from western Japan. J. Phycol. 2011, 47
47. Varkitzi, I.; Pagou, K.; Graneli, E.; Hatzianestis, I.; Pyrgaki, C.; Pavlidou, A.; Montesanto, B.; Economou-Amilli, A. Unbalanced N:P ratios and nutrient stress controlling growth and toxin production of the harmful dinoflagellate Prorocentrum lima (Ehrenberg) Dodge. Harmful Algae 2010, 9, 304-311.
48. Medhioub, A.; Medhioub, W.; Amzil, Z.; Sibat, M.; Bardouil, M.; Ben Neila, I.; Mezghani, S.; Hamza, A.; Lassus, P. Influence of environmental parameters on Karenia selliformis toxin content in culture. Cah. Biol. Mar. 2009, 50, 333-342.
49. Pizarro, G.; Paz, B.; Gonzalez-Gil, S.; Franco, J.M.; Reguera, B. Seasonal variability of lipophilic toxins during a Dinophysis acuta bloom in Western Iberia: Differences between picked cells and plankton concentrates. Harmful Algae 2009, 8, 926-937.
50. Parker, N.S.; Negri, A.P.; Frampton, D.M.F.; Rodolfi, L.; Tredici, M.R.; Blackburn, S.I. Growth of the toxic dinoflagellate Alexandrium minutum (Dinophyceae) using high biomass culture systems. J. Appl. Phycol. 2002, 14, 313-324. (Pubitemid 36189282)
51. Gallardo Rodriguez, J.J.; Sanchez Miron, A.; Garcia Camacho, F.; Ceron Garcia, M.C.; Belarbi, E.H.; Molina Grima, E. Culture of dinoflagellates in a fed-batch and continuous stirred-tank photobioreactors: Growth, oxidative stress and toxin production. Process Biochem. 2010, 45, 660-666.
52. Jauffrais, T.; Herrenknecht, C.; Séchet, V.; Sibat, M.; Tillmann, U.; Krock, B.; Kilcoyne, J.; Miles, C.O.; McCarron, P.; Amzil, Z.; et al. Quantitative analysis of azaspiracids in Azadinium spinosum cultures. Anal. Bioanal. Chem. 2012, 403, 833-846.
53. MacKenzie, L.; Beuzenberg, V.; Holland, P.; McNabb, P.; Selwood, A. Solid phase adsorption toxin tracking (SPATT): A new monitoring tool that simulates the biotoxin contamination of filter feeding bivalves. Toxicon 2004, 44, 901-918. (Pubitemid 39504922)
54. Fux, E. Development and evaluation of passive sampling and LC-MS based techniques for the detection and monitoring of lipophilic marine toxins in mesocosm and field studies. Ph.D. Thesis, Dublin Institute of Technology, Dublin, Ireland, 2008.
55. Fux, E.; Marcaillou, C.; Mondeguer, F.; Bire, R.; Hess, P. Field and mesocosm trials on passive sampling for the study of adsorption and desorption behaviour of lipophilic toxins with a focus on OA and DTX1. Harmful Algae 2008, 7, 574-583.
56. Fux, E.; Bire, R.; Hess, P. Comparative accumulation and composition of lipophilic marine biotoxins in passive samplers and in mussels (M. edulis) on the West Coast of Ireland. Harmful Algae 2009, 8, 523-537.
57. MacKenzie, L.A. In situ passive solid-phase adsorption of micro-algal biotoxins as a monitoring tool. Curr. Opin. Biotechnol. 2010, 21, 326-331.
58. Alfonso, C.; Rehmann, N.; Hess, P.; Alfonso, A.; Wandscheer, C.B.; Abuin, M.; Vale, C.; Otero, P.; Vieytes, M.R.; Botana, L.M. Evaluation of various pH and temperature conditions on the stability of azaspiracids and their importance in preparative isolation and toxicological studies. Anal. Chem. 2008, 80, 9672-9680.
59. Keller, M.D.; Selvin, R.C.; Claus, W.; Guillard, R.R.L. Media for the culture of oceanic ultraphytoplankton. J. Phycol. 1987, 23,
60. Quilliam, M. A.; Hess, P.; Dell'Aversano, C. Recent Developments in the Analysis of Phycotoxins by Liquid Chromatography-Mass Spectrometry. In Mycotoxins and Phycotoxins in Perspective at the turn of the Millenium: Proceedings of the Xth International IUPAC Symposium on Mycotoxins and Phycotoxins, Guaruja, Brazil; de Koe, W.J., Sampson, R.A., van Egmond, H.P., Gilbert, J., Sabinoan, M., Eds.; IUPAC: Research Triangle Park, NC, USA, 2001; pp. 383-391.
61. Jauffrais, T.; Marcaillou, C.; Herrenknecht, C.; Truquet, P.; Séchet, V.; Nicolau, E.; Tillmann, U.; Hess, P. Azaspiracid accumulation, detoxification and biotransformation in blue mussels (Mytilus edulis) experimentally fed Azadinium spinosum. Toxicon 2012, doi:10.1016/j.toxicon.2012. 04.351.