Characterization of nontoxic and toxin-producing strains of Alexandrium minutum (Dinophyceae) in Irish coastal waters

Applied and Environmental Microbiology

Volumn 73, Issue 10, 2007, Pages 3333-3342

  Touzet, Nicolas ^a   Franco, Jose M ^b   Raine, Robin ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b INSTITUTO ESPAÑOL DE OCEANOGRAFÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CLONING; DNA SEQUENCES; POLYMORPHISM; SEAWATER; TOXIC MATERIALS;

CLONAL CULTURES; COASTAL WATERS; PARALYTIC SHELLFISH POISONING (PSP);

MARINE BIOLOGY;

RIBOSOME DNA; SHELLFISH TOXIN;

COASTAL WATER; COMPARATIVE STUDY; CYST; DINOFLAGELLATE; DNA FINGERPRINTING; LIQUID CHROMATOGRAPHY; MORPHOLOGY; TOXIN; WATER COLUMN;

ALEXANDRIUM MINUTUM; ARTICLE; CELL STRUCTURE; COASTAL WATERS; DINOFLAGELLATE; DNA SEQUENCE; FLUORESCENCE; GENETIC POLYMORPHISM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IRELAND; NONHUMAN; NUCLEOTIDE SEQUENCE; RANDOM AMPLIFIED POLYMORPHIC DNA; SHELLFISH POISONING; TOXIN ANALYSIS;

ANIMALS; CLUSTER ANALYSIS; DINOFLAGELLIDA; DNA FINGERPRINTING; DNA, PROTOZOAN; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; GENES, RRNA; IRELAND; MARINE TOXINS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; RNA, RIBOSOMAL, 28S; RNA, RIBOSOMAL, 5.8S; SEAWATER; SEQUENCE HOMOLOGY, NUCLEIC ACID; VARIATION (GENETICS); WATER MICROBIOLOGY;

CONNACHT; CORK HARBOUR; COUNTY CORK; COUNTY GALWAY; EURASIA; EUROPE; IRELAND; KILLARY HARBOUR; MUNSTER [IRELAND]; WESTERN EUROPE;

ALEXANDRIUM MINUTUM; DINOPHYCEAE;

EID: 34249659502     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02161-06     Document Type: Article

References (67)

1. Adachi, M., Y. Sako, and Y. Ishida. 1996. Analysis of Alexandrium (Dinophyceae) species using sequences of the 5.8S ribosomal DNA and internal transcribed spacer regions. J. Phycol. 32:424-432.
2. Adachi, M., Y. Sako, and Y. Ishida. 1997. Analysis of Gymnodinium catenatum Dinophyceae using sequences of the 5.8S rDNA-ITS regions and random amplified polymorphic DNA. Fish Sci. 63:701-707.
3. Anderson, D. M. 1997. Bloom dynamics of toxic Alexandrium species in the northeastern U.S. Limnol. Oceanogr. 42:1009-1022.
4. Anderson, D. M., D. M. Kulis, G. J. Doucette, J. C. Gallagher, and E. Balech. 1994. Biogeography of toxic dinoflagellates in the genus Alexandrium from the northeastern United States and Canada. Mar. Biol. 120:467-478.
5. Anderson, D. M., D. M. Kulis, and B. A. Keafer. 1999. Detection of the toxic dinoflagellate Alexandrium fundyense (Dinophyceae) with oligonucleotide and antibody probes; variability in labelling intensity with physiological condition. J. Phycol. 35:870-883.
6. Balech, E. 1989. Redescription of Alexandrium minutum Halim (Dinophyceae) type species of the genus Alexandrium. Phycologia 28:206-211.
7. Balech, E. 1995. The genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine Station, Sherkin Island Co., Cork, Ireland.
8. Biegala, I. C., G. Kennaway, E. Alverca, J.-F. Lennon, D. Vaulot, and N. Simon. 2002. Identification of bacteria associated with dinoflagellates (Dinophyceae) Alexandrium spp. using tyramide signal amplification- fluorescent in situ hybridization and confocal microscopy. J. Phycol. 38:404-411.
9. Boelens, R. G. V., D. M. Maloney, A. P. Parsons, and A. R. Walsh. 1999. Ireland's marine and coastal areas and adjacent sea: an environmental assessment. Marine Institute, Dublin, Ireland.
10. Bolch, C. J. S., S. I. Blackburn, G. M. Hallegraeff, and R. E. Vaillancourt. 1999. Genetic variation among strains of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). J. Phycol. 35:356-367.
11. Bolch, C. J. S., A. P. Negri, and G. M. Hallegraeff. 1999. Gymnodinium microreticulatum sp. nov. (Dinophyceae): a naked, microreticulate cyst-producing dinoflagellate, distinct from Gymnodinium catenatum and Gymnodinium nolleri. Phycologia 38:301-313.
12. Bornet, B., E. Antoine, E. Francoise, and C. Marcaillou-Le Baut. 2005. Development of sequence characterized amplified region markers from intersimple sequence repeat fingerprintings for the molecular detection of toxic phytoplankton Alexandrium catenella (Dinophyceae) and Pseudonitzschia pseudodelicatissima (Bacillariophyceae) from French coastal waters. J. Phycol. 41:704-711.
13. Camino Ordas, M., S. Fraga, J. M. Franco, A. Ordas, and A. Figueras. 2004. Toxin and molecular analysis of Gymnodinium catenatum (Dinophyceae) strains from Galicia (NW Spain) and Andalucia (S Spain). J. Plankton Res. 26:341-349.
14. Cembella, A. D., J. J. Sullivan, G. L. Boyer, F. J. R. Taylor, and R. J. Andersen. 1987. Variation in paralytic shellfish toxin composition within the Protogonyaulax tamarensis/catenella species complex; red tide dinoflagellates. Biochem. Syst. Ecol. 15:171-186.
15. Chang, F. H., D. M. Anderson, D. M. Kulis, and D. J. Till. 1997. Toxin production of Alexandrium minutum (Dinophyceae) from the Bay of Plenty, New Zealand. Toxicon 35:393-409.
16. Dantzer, W. R., and R. E. Levin. 1997. Bacterial influence on the production of paralytic shellfish toxins by dinoflagellated algae. J. Appl. Microbiol. 83:464-469.
17. Franco, J. M., and P. Fernandez Vila. 1993. Separation of paralytic shellfish toxins by reversed phase high performance liquid chromatography with post-column reaction and fluorimetric detection. Chromatographia 35:613-620.
18. Fritz, L., and R. E. Triemer. 1985. A rapid simple technique utilizing Calcofluor White M2R for the visualization of dinoflagellate thecal plates. J. Phycol. 21:662-664.
19. Furey, A., K. J. James, and I. R. Sherlock. 1998. First report of paralytic shellfish poisoning toxins in the Republic of Ireland, p. 70-71. In B. Reguera, J. Blanco, M. L. Fernandez, and T. Wyatt (ed.), Harmful algae. Xunta de Galicia and IOC of UNESCO, Santiago de Compostela, Spain.
20. Gallacher, S., K. J. Flynn, J. M. Franco, E. E. Brueggemann, and H. B. Hines. 1997. Evidence for production of paralytic shellfish toxins by bacteria associated with Alexandrium spp. (Dinophyta) in culture. Appl. Environ. Microbiol. 63:239-245.
21. Galluzzi, L., A. Penna, E. Bertozzini, M. Vila, E. Garces, and M. Magnani. 2004. Development of a real-time PCR assay for rapid detection and quantification of Alexandrium minutum (a dinoflagellate). Appl. Environ. Microbiol. 70:1199-1206.
22. Godhe, A., S. K. Otta, H. A. S. Rehnstam, I. Karunasagar, and I. Karunasagar. 2001. Polymerase Chain Reaction in detection of Gymnodinium mikimotoi and Alexandrium minutum in field samples from Southwest India. Mar. Biotechnol. 3:152-162.
23. Guillard, R. 1975. Culture of phytoplankton for feeding marine invertebrates, p. 29-60. In W. Smith and M. H. Chanley (ed.), Culture of marine invertebrate animals. Plenum Press, New York, NY.
24. Hallegraeff, G. M. 1993. A review of harmful algal blooms and the apparent global increase. Phycologia 32:79-99.
25. Hallegraeff, G. M., D. A. Steffensen, and R. Wetherbee. 1988. Three estuarine dinoflagellates that can produce paralytic shellfish toxins. J. Plankton Res. 10:533-541.
26. Hansen, G., N. Daugbjerg, and J. M. Franco. 2003. Morphology, toxin composition and LSU rDNA phylogeny of Alexandrium minutum (Dinophyceae) from Denmark, with some morphological observations on other European strains. Harmful Algae 2:317-335.
27. Higman, W. A., D. M. Stone, and J. M. Lewis. 2001. Sequence comparison of toxic and non-toxic Alexandrium tamarense (Dinophyceae) isolates from UK waters. Phycologia 40:256-262.
28. Hosoi-Tanabe, S., and Y. Sako. 2004. Rapid detection of natural cells of Alexandrium tamarense and A. catenella (Dinophyceae) by fluorescence in situ hybridization. Harmful Algae 4:319-328.
29. Hwang, D. F., and Y. H. Lu. 2000. Influence of environmental and nutritional factors on growth, toxicity, and toxin profile of dinoflagellate Alexandrium minutum. Toxicon 38:1491-1503.
30. John, U., A. Cembella, C. Hummert, M. Elbrachter, R. Groben, and L. Medlin. 2003. Discrimination of the toxigenic dinoflagellates Alexandrium tamarense and A. ostenfeldii in co-occurring natural populations from Scottish coastal waters. Eur. J. Phycol. 38:25-40.
31. John, U., R. A. Fensome, and L. K. Medlin. 2003. The application of a molecular clock based on molecular sequences and the fossil record to explain biogeographic distributions within the Alexandrium tamarense "species complex" (Dinophyceae). Mol. Biol. Evol. 20:1015-1027.
32. John, U., R. Groben, B. Beszteri, and L. Medlin. 2004. Utility of amplified fragment length polymorphisms (AFLP) to analyze genetic structures within the Alexandrium tamarense species complex. Protist 155:169-179.
33. Kao, C. Y. 1993. Paralytic shellfish poisons, p. 75-86. In I. R. Falconer (ed.), Algal toxins in seafood and drinking waters. Academic Press, London, United Kingdom.
34. Lenaers, G., L. Maroteaux, B. Michot, and M. Herzog. 1989. Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA. J. Mol. Evol. 29:40-51.
35. Lewis, J., G. Kennaway, S. Franca, and E. Alverca. 2001. Bacterium-dinoflagellate interactions: investigative microscopy of Alexandrium spp. (Gonyaulacales, Dinophyceae). Phycologia 40:280-285.
36. Lilly, E. L., D. M. Kulis, P. Gentien, and D. M. Anderson. 2002. Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from the western Pacific: evidence from DNA and toxin analysis. J. Plankton Res. 24:443-452.
37. Lilly, E. L., K. M. Halanych, and D. M. Anderson. 2005. Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae 4:1004-1020.
38. Lippemeier, S., D. M. F. Frampton, S. I. Blackburn, S. Geier, and A. P. Negri. 2003. Influence of phosphorus limitation on toxicity and photosynthesis of Alexandrium minutum (Dinophyceae) monitored by in-line detection of variable chlorophyll fluorescence. J. Phycol. 38:320-331.
39. Martinez, R., C. Anibarro, and S. Fernandez. 2006. Genetic variability among Alexandrium tamarense and Alexandrium minutum strains studied by RAPD banding pattern analysis. Harmful Algae 5:599-607.
40. McDermott, G., and R. Raine. 2006. The dinoflagellate genus Ceratium in Irish shelf seas. The Martin Ryan Institute, Galway, Ireland.
41. McMahon, T. G., R. C. T. Raine, T. Fast, L. Kies, and J. W. Patching. 1992. Phytoplankton biomass, light attenuation and mixing in the Shannon Estuary, Ireland. J. Mar. Biol. 72:709-720.
42. Murayama-Sadaaki, E., S. Yoshimatsu, T. Kayano, T. Nishio, H. Ueda, and T. Nagamune. 1998. Application of the random amplified polymorphic DNA (RAPD) technique to distinguishing species of the red tide phytoplankton Chattonella (Raphydophyceae). J. Ferment. Bioeng. 85:343-345.
43. Montresor, M., U. John, A. Beran, and L. K. Medlin. 2004. Alexandrium tamutum sp. nov. (Dinophyceae): a new nontoxic species in the genus Alexandrium. J. Phycol. 40:398-411.
44. Nagai, S., C. Lian, M. Hamaguchi, Y. Matsuyama, S. Itakura, and T. Hogetsu. 2004. Development of microsatellite markers in the toxic dinoflagellate Alexandrium tamarense (Dinophyceae). Mol. Ecol. Notes 4:83-85.
45. Nascimento, S. M., D. A. Purdie, E. L. Lilly, J. Larsen, and S. Morris. 2005. Toxin profile, pigment composition, and large subunit rDNA phylogenetic analysis of an Alexandrium minutum (Dinophyceae) strain isolated from the Fleet Lagoon, United Kingdom. J. Phycol. 41:343-353.
46. Oshima, Y., K. Sugino, and T. Yasumoto. 1989. Latest advances in HPLC analysis of paralytic shellfish toxins, p. 319-326. In S. Natori, K. Hashimoto, and Y. Ueno (ed.), Mycotoxins and phycotoxins '88. Elsevier, Amsterdam, The Netherlands.
47. Penna, A., E. Garces, M. Vila, M. G. Giacobbe, S. Fraga, A. Luglie, I. Bravo, E. Bertozzini, and C. Vernesi. 2005. Alexandrium catenella (Dinophyceae), a toxic ribotype expanding in the NW Mediterranean Sea. Mar. Biol. 148:13-23.
48. Percy, L., W. Higman, D. Stone, S. Morris, and J. Lewis. 2004. A detailed study of phytoplankton in the Fal Estuary, U.K., and the relationship between Alexandrium species and PSP toxin profiles of Mytilus edulis, p. 12. Abstr. 5th Int. Conf. Molluscan Shellfish Safety, Galway, Ireland, 14 to 18 June 2004.
49. Posada, D., and K. A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818.
50. Raine, R., and T. McMahon. 1998. Physical dynamics on the continental shelf off southwestern Ireland and their influence on coastal phytoplankton blooms. Cont. Shelf Res. 18:883-914.
51. Roden, C. M., P. G. Rodhouse, M. P. Hensey, T. McMahon, T. H. Ryan, and J. P. Mercer. 1987. Hydrography and the distribution of phytoplankton in Killary Harbour: a fjord in western Ireland. J. Mar. Biol. 67:359-371.
52. Sako, Y., C. M. Adachi, and Y. Ishida. 1993. Preparation of characterization of monoclonal antibodies to Alexandrium species, p. 87-93. In T. J. Smayda and Y. Shimizu (ed.), Toxic phytoplankton blooms in the sea. Elsevier, New York, NY.
53. Sako, Y., H. Kim, H. Ninomiya, M. Adachi, and Y. Ishida. 1990. Isozyme and cross analysis of mating populations in the Alexandrium catenella/tamarense species complex, p. 320-323. In E. Graneli, E. Sunderstrom, L. Edler, and D. M. Anderson (ed.), Toxic marine phytoplankton. Elsevier, New York, NY.
54. Scholin, C. A., G. M. Hallegraeff, and D. M. Anderson. 1995. Molecular evolution of the Alexandrium tamarense species complex (Dinophyceae): dispersal in the North American and west Pacific regions. Phycologia 34: 472-485.
55. Scholin, C. A., M. Herzog, M. Sogin, and D. M. Anderson. 1994. Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30:999-1011.
56. Shrestha, M. K., A. Golan-Goldhirsh, and D. Ward. 2002. Population genetic structure and the conservation of isolated populations of Acacia raddiana in the Negev Desert. Biol. Conserv. 108:119-127.
57. Simon, N., I. C. Biegala, E. A. Smith, and D. Vaulot. 2002. Kinetics of attachment of potentially toxic bacteria to Alexandrium tamarense. Aquat. Microb. Ecol. 28:249-256.
58. Simon, N., L. Campbell, E. Ornolfsdottir, R. Groben, L. Guillou, M. Lange, and L. K. Medlin. 2000. Oligonucleotide probes for the identification of three algal groups by dot blot and fluorescent whole-cell hybridization. J. Eukaryot. Microbiol. 47:76-84.
59. Spalter, R. A., D. Walsh, R. A. Reeves, D. J. Saul, R. D. Gray, P. L. Bergquist, L. McKenzie, and P. R. Bergquist. 1997. Sequence heterogeneity of the ribosomal RNA intergenic region Alexandrium species. Biochem. Syst. Ecol. 25:231-239.
60. Swofford, D. L. 2002. PAUP* phylogenetic analysis using parsimony, version 4.0b10. Sinauer Associates, Sunderland, MA.
61. Tengs, T., H. A. Bowers, H. B. Glasgow, Jr., J. M. Burkholder, and D. W. Oldach. 2003. Identical ribosome DNA sequence data from Pfiesteria piscicida (Dinophyceae) isolates with different toxicity phenotypes. Environ. Res. 93:88-91.
62. Tillmann, U., and U. John. 2002. Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defense mechanism independent of PSP-toxin content. Mar. Ecol. Prog. Ser. 230:47-58.
63. Touzet, N., B. Paz Pino, P. Riobó Agulla, J. M. Franco, and R. Raine. 2004. Abstr. 5th Int. Conf. Molluscan Shellfish Safety, abstr. 120.
64. Usup, G., L. C. Pin, A. Ahmad, and L. P. Teen. 2002. Phylogenetic relationship of Alexandrium tamiyavanichii (Dinophyceae) to other Alexandrium species based on ribosomal RNA gene sequences. Harmful Algae 1:59-68.
65. Usup, G., L. C. Pin, A. Ahmad, and L. P. Teen. 2002. Alexandrium (Dinophyceae) species in Malaysia waters. Harmful Algae 1:265-275.
66. Walsh, D., R. A. Reeves, D. J. Saul, R. D. Gray, L. Mackenzie, P. R. Berquist, and P. L. Bergquist. 1998. Heterogeneity of SSU and LSU rDNA sequences of Alexandrium species. Biochem. Syst. Ecol. 26:495-509.
67. Wang, X. L., Y. X. Yang, Y. Z. Cong, and D. L. Duan. 2004. DNA finger-printing of selected Laminaria (Phaeophyta) gametophytes by RAPD markers. Aquaculture 238:143-153.