Strain variation in karlodinium veneficum (dinophyceae): Toxin profiles, pigments, and growth characteristics

Journal of Phycology

Volumn 45, Issue 1, 2009, Pages 137-153

  Bachvaroff, Tsvetan R ^a   Adolf, Jason E ^a   Place, Allen R ^a  

^a Center of Marine Biotechnology   (United States)

Author keywords

Growth; Karlodinium; Karlotoxin; Pigments; Strain

Indexed keywords

BACTERIA (MICROORGANISMS); DINOPHYCEAE; KARLODINIUM;

EID: 60349095662     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2008.00629.x     Document Type: Article

References (43)

1. Adolf, J. E., Bachvaroff, T. R., Krupatkina, D. N., Nonogaki, H., Brown, P. J. P., Lewitus, A. J., Harvey, H. R. Place, A. R. 2006. Species specificity and potential roles of Karlodinium micrum toxin. Afr. J. Mar. Sci. 28 : 415 21.
2. Adolf, J. E., Bachvaroff, T. R., Krupatkina, D. N. Place, A. R. 2007. Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae 6 : 400 12.
3. Adolf, J. E., Bachvaroff, T. R. Place, A. R. 2008a. Manger à trois: toxic vs. non-toxic Karlodinium veneficum strains with a predator, Oxyrrhis marina, and prey, Storeatula major. In Moestrup, Ø. Ed Proceedings of the 12th International Conference on Harmful Algae, Copenhagen, Denmark, pp. 107 10.
4. Adolf, J. E., Bachvaroff, T. Place, A. R. 2008b. Can cryptophyte abundance triger toxic Karlodinium veneficum blooms in eutrophic estuaries? Harmful Algae 8 : 119 28.
5. Adolf, J. E., Bachvaroff, T. R. Place, A. R. 2009. Environmental modulation of karlotoxin levels in strains of the cosmopolitan dinoflagellate Karlodinium veneficum (Dinophyceae). J. Phycol. (in press).
6. Andersen, R. A., Morton, S. L. Sexton, J. P. 1997. Provasoli-Guillard national center for culture of marine phytoplankton 1997 list of strains. J. Phycol. 33 (Suppl. 1 75.
7. Arzul, G., Gentein, P. Crassous, M. 1994. A haemolytic test to assay toxins excreted by the marine dinoflagellate Gyrodinium cf. aureolum. Water Res. 28 : 961 5.
8. Bachvaroff, T. R., Adolf, J. E. Place, A. R. 2008b. Phylogeography of Atlantic Coast Karlodinium veneficum strains: a genetic marker correlates with toxin type. In Moestrup, Ø. Ed Proceedings of the 12th International Conference on Harmful Algae, Copenhagen, Denmark, pp. 55 8.
9. Bachvaroff, T. R., Adolf, J. E., Squier, A., Harvey, H. R. Place, A. R. 2008a. Liquid chromatographic-mass spectroscopic characterization, detection, and quantification of karlotoxins. Harmful Algae 7 : 473 84.
10. Bai, X., Adolf, J. E., Bachvaroff, T., Place, A. R. Coats, D. W. 2007. The interplay between host toxin and parasitism by Amoebophrya. Harmful Algae 6 : 670 8.
11. Ballantine, D. 1956. Two new marine species of Gymnodinium isolated from the Plymouth area. J. Mar. Biol. Assoc. U. K. 35 : 467 74.
12. Bergholtz, T., Daugbjerg, N., Moestrup, Ø. Ferna′ndez- Tejedor, M. 2005. On the identity of Karlodinium veneficum and description of Karlodinium arminger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. J. Phycol. 42 : 170 93.
13. Bjørnland, T., Fiksdahl, A., Skjetne, T., Krane, J. Liaaen-Jensen, S. 2000. Gyroxanthin - the first allenic acetylenic carotenoid. Tetrahedron 56 : 9047 56.
14. Blackburn, S. I., Bolch, C. J., Haskard, K. A. Hallegraeff, G. M. 2001. Reproductive compatibility among four global populations of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). Phycologia 40 : 78 87.
15. Bolch, C. J., Orr, P. T., Jones, G. J. Blackburn, S. I. 1999. Genetic, morphological, and toxicological variation among globally distributed strains of Nodularia (Cyanobacteria). J. Phycol. 35 : 339 55.
16. Bomber, J. W., Tindall, D. R. Miller, D. M. 1989. Genetic variability in toxin potencies among seventeen clones of Gambierdiscus toxicus (Dinophyceae). J. Phycol. 25 : 617 25.
17. Brownlee, E. F., Sellner, S. G., Sellner, K. G., Nonogaki, H., Adolf, J. E., Bachvaroff, T. R. Place, A. R. 2008. Responses of Crassostrea virginica (Gmelin) and C. ariakensis (Fujita) to bloom-forming phytoplankton including ichthyotoxic Karlodinium veneficum (Ballantine). J. Shellfish Res. 27 : 581 91.
18. Cho, E. S. Lee, H. J. 2001. Thecal plates, toxin content and growth of five clones of Alexandrium tamarense (Dinophyceae) isolated from Jinhae Bay, Korea. Phycologia 40 : 435 9.
19. Costas, E. 1990. Genetic variability in growth rates of marine dinoflagellates. Genetica 82 : 99 102.
20. Daugbjerg, N., Hansen, G., Larsen, J. Moestrup, Ø. 2000. Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39 : 302 17.
21. Deeds, J. R., Kibler, S. R., Tester, P. A. Place, A. R. 2004. Geographic strain variation in toxin production in Karlodinium micrum (Dinophyceae) from southeastern United States. In Steidinger, K. A., Landsberg, J. H., Tomas, C. R. Vargo, G. A. Eds Harmful Algae 2002 Proceedings. Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St. Petersberg, pp. 145 7.
22. Deeds, J. Place, A. R. 2006. Sterol-specific membrane interactions with the toxins from Karlodinium micrum (Dinophyceae) - a strategy for self-protection? Afr. J. Mar. Sci. 28 : 421 5.
23. Deeds, J. R., Reimschussel, R. Place, A. R. 2006. Histopathological effects in fish exposed to the toxins from Karlodinium micrum (Dinophyceae). J. Aquat. Anim. Health 18 : 136 48.
24. Deeds, J. R., Terlizzi, D. E., Adolf, J. E., Stoecker, D. K. Place, A. R. 2002. Toxic activity from cultures of Karlodinium micrum (=Gyrodinium galatheanum) (Dinophyceae) - a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae 1 : 169 89.
25. Doyle, J. J. Doyle, J. L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19 : 11 15.
26. Evans, K. M., Bates, S. S., Medlin, L. K. Hayes, P. K. 2004. Microsatellite marker development and genetic variation in the toxic marine diatom Pseudo-nitzschia multiseries (Bacillariophyceae). J. Phycol. 40 : 911 20.
27. Fensin, E. E. 2004. Occurrence and ecology of the dinoflagellate Karlodinium micrum in estuaries of North Carolina, USA. In Steidinger, K. A., Landsberg, J. H., Tomas, C. R. Vargo, G. A. Eds Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St. Pete's, Florida, pp. 62 4.
28. Goshorn, D., Deeds, J., Tango, P., Poukish, C., Place, A. R., McGinty, M., Butler, W., Luckett, C. Magnien, R. 2004. Occurrence of Karlodinium micrum and its association with fish kills in Maryland estuaries. In Steidinger, K. A., Landsberg, J. H., Tomas, C. R. Vargo, G. A. Eds Proceedings of Harmful Algae 2002. Florida Fish and Wildlife Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St. Petersberg, pp. 361 3.
29. Guillo, L., Nezan, E., Cueff, V., Erard-Le Denn, E., Cambon-Bonavita, M.-A., Gentien, P. Barbier, G. 2002. Genetic diversity and molecular detection of three dinoflagellate genera (Alexandrium, Dinophysis, and Karenia) from French coasts. Protist 153 : 223 38.
30. Hall, N. S., Litaker, R. W., Fensin, E., Adolf, J. E., Bowers, H. A., Place, A. R. Paerl, H. W. 2008. Environmental factors contributing to the development and demise of a toxic dinoflagellate (Karlodinium veneficum) bloom in a shallow, eutrophic, lagoonal estuary. Estuar. Coasts 31 : 402 18.
31. Johnsen, G. Sakshaug, E. 1993. Bio-optical characteristics and photoadaptive responses in the toxic and bloom-forming dinoflagellates Gyrodinium aureolum, Gymnodinium galatheanum, and two strains of Prorocentrum minimum. J. Phycol. 29 : 627 42.
32. Johnson, M. D., Rome, M. Stoecker, D. S. 2003. Microzooplankton grazing on Prorocentrum minimum and Karlodinium micrum in Chesapeake Bay. Limnol. Oceanogr. 48 : 238 48.
33. Kempton, J. W., Lewitus, A. J., Deeds, J. R., Law, J. M. Place, A. R. 2002. Toxicity of Karlodinium micrum (Dinophyceae) associated with a fish kill in a South Carolina brackish retention pond. Harmful Algae 1 : 233 41.
34. Li, A., Adolf, J. E. Stoecker, D. K. 1999. Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat. Microb. Ecol. 19 : 163 76.
35. Litaker, R. W., Vandersea, M. W., Kibler, S. R., Reece, K. S., Stokes, N. A., Steidinger, K. A., Millie, D. F., Bendis, B. J., Pigg, R. J. Tester, P. A. 2003. Identification of Pfiesteria piscicida (Dinophyceae) and Pfiesteria-like organsims using internal transcribed spacer-specific PCR assays. J. Phycol. 39 : 754 61.
36. Schmidt, L. E. Hansen, P. J. 2001. Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH. Mar. Ecol. Prog. Ser. 216 : 67 81.
37. Scholin, C., Villac, M. C., Buck, K., Krupp, J. M., Powers, D. A., Fryxell, G. A. Chavez, F. 1994. Ribosomal DNA sequences discriminate among toxic and non-toxic Pseudo-nitzschia species. Nat. Toxins 2 : 152 65.
38. Stoecker, D. K., Adolf, J. E., Place, A. R., Glibert, P. M. Meritt, D. 2008. Effects of the dinoflagellates Karlodinium veneficum and Prorocentrum minimum on early life history stages of the Eastern Oyster, Crassostrea virginica. Mar. Biol. 154 : 81 90.
39. Stolte, W., Kraay, G. W., Noordeloos, A. A. M. Riegman, R. 2000. Genetic and physiological variation in pigment composition of Emiliania huxleyi (Prymnesiophyceae) and the potential use of its pigment ratios as a quantitative physiological marker. J. Phycol. 36 : 529 39.
40. Tengs, T., Bowers, H. A., Ziman, A. P., Stoecker, D. K. Oldach, D. W. 2001. Genetic polymorphism in Gymnodinium galatheanum chloroplast DNA sequences and development of a molecular detection assay. Mol. Ecol. 10 : 515 23.
41. Van Heukelem, L. Thomas, C. S. 2001. Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments. J. Chromatogr. A 910 : 31 49.
42. Waggett, R. J., Tester, P. A. Place, A. R. 2008. Anti-grazing properties of toxic Karlodinium veneficum: karlotoxin as a grazing deterrent in predator-prey interactions with the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 366 : 31 42.
43. Wilson, A. E., Sarnelle, O., Nelan, B. A., Salmon, T. P., Gehringer, M. M. Hay, M. E. 2005. Genetic variation of the bloom-forming cyanobacterium Microcystis aeruginosa within and among lakes: implications for harmful algal blooms. Appl. Environ. Microbiol. 71 : 6126 33.