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Bioluminescence capability and intensity in the dinoflagellate Alexandrium species

  • Park, Sang Ah (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Ok, Jin Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Kang, Hee Chang (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • You, Ji Hyun (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Eom, Se Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Yoo, Yeong Du (Department of Marine Biotechnology, College of Ocean Sciences, Kunsan National University) ;
  • Lee, Moo Joon (Department of Marine Biotechnology, Anyang University)
  • 투고 : 2021.10.30
  • 심사 : 2021.12.06
  • 발행 : 2021.12.15

초록

Some species in the dinoflagellate genus Alexandrium are bioluminescent. Of the 33 formally described Alexandrium species, the bioluminescence capability of only nine species have been tested, and eight have been reported to be bioluminescent. The present study investigated the bioluminescence capability of seven Alexandrium species that had not been tested. Alexandrium mediterraneum, A. pohangense, and A. tamutum were bioluminescent, but A. andersonii, A. hiranoi, A. insuetum, and A. pseudogonyaulax were not. We also measured the bioluminescent intensity of A. affine, A. fraterculus, A. mediterraneum, A. ostenfeldii, A. pacificum, A. pohangense, A. tamarense, and A. tamutum. The mean 200-second-integrated bioluminescence intensity per cell ranged from 0.02 to 32.2 × 104 relative luminescence unit per cell (RLU cell-1), and the mean maximum bioluminescence intensity per cell per second (BLMax) ranged from 0.01 to 10.3 × 104 RLU cell-1 s-1. BLMax was significantly correlated with the maximum growth rates of Alexandrium species, except for A. tamarense. A phylogenetic tree based on large subunit ribosomal DNA (LSU rDNA) showed that the bioluminescent species A. affine, A. catenella, A. fraterculus, A. mediterraneum, A. pacificum, and A. tamarense formed a large clade. However, the toxicity or mixotrophic capability of these species was split. Thus, their bioluminescence capability in this clade was more consistent than their toxicity or mixotrophic capability. Phylogenetic trees based on LSU rDNA and the luciferase gene of Alexandrium were consistent except for A. pohangense. The results of the present study can provide a basis for understanding the interspecific diversity in bioluminescence of Alexandrium.

키워드

과제정보

This research was supported by the National Research Foundation (NRF) funded by the Ministry of Science and ICT (NRF-2020M3F6A1110582; NRF-2021M3I6A1091272; 2021R1A2C1093379) and by the Useful Dinoflagellate program of Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) award to HJJ.

참고문헌

  1. Anderson, D. M., Alpermann, T. J., Cembella, A. D., Collos, Y., Masseret, E. & Montresor, M. 2012. The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10-35. https://doi.org/10.1016/j.hal.2011.10.012
  2. Baker, A., Robbins, I., Moline, M. A. & Iglesias-Rodriguez, M. D. 2008. Oligonucleotide primers for the detection of bioluminescent dinoflagellates reveal novel luciferase sequences and information on the molecular evolution of this gene. J. Phycol. 44:419-428. https://doi.org/10.1111/j.1529-8817.2008.00474.x
  3. Bergkvist, J., Selander, E. & Pavia, H. 2008. Induction of toxin production in dinoflagellates: the grazer makes a difference. Oecologia 156:147-154. https://doi.org/10.1007/s00442-008-0981-6
  4. Biggley, W. H., Swift, E., Buchanan, R. J. & Seliger, H. H. 1969. Stimulable and spontaneous bioluminescence in the marine dinoflagellates, Pyrodinium bahumense, Gonyaulax polyedra, and Pyrocystis lunula. J. Gen. Physiol. 54:96-122. https://doi.org/10.1085/jgp.54.1.96
  5. Bill, B. D., Moore, S. K., Hay, L. R., Anderson, D. M. & Trainer, V. L. 2016. Effects of temperature and salinity on the growth of Alexandrium (Dinophyceae) isolates from the Salish Sea. J. Phycol. 52:230-238. https://doi.org/10.1111/jpy.12386
  6. Blossom, H. E., Baedkel, T. D., Tillmann, U. & Hansen, P. J. 2017. A search for mixotrophy and mucus trap production in Alexandrium spp. and the dynamics of mucus trap formation in Alexandrium pseudogonyaulax. Harmful Algae 64:51-62. https://doi.org/10.1016/j.hal.2017.03.004
  7. Blossom, H. E., Daugbjerg, N. & Hansen, P. J. 2012. Toxic mucus traps: a novel mechanism that mediates prey uptake in the mixotrophic dinoflagellate Alexandrium pseudogonyaulax. Harmful Algae 17:40-53. https://doi.org/10.1016/j.hal.2012.02.010
  8. Blossom, H. E., Markussen, B., Daugbjerg, N., Krock, B., Norlin, A. & Hansen, P. J. 2019. The cost of toxicity in microalgae: direct evidence from the dinoflagellate Alexandrium. Front. Microbiol. 10:1065. https://doi.org/10.3389/fmicb.2019.01065
  9. Ciminiello, P., Fattorusso, E., Forino, M. & Montresor, M. 2000. Saxitoxin and neosaxitoxin as toxic principles of Alexandrium andersoni (Dinophyceae) from the Gulf of Naples, Italy. Toxicon 38:1871-1877. https://doi.org/10.1016/S0041-0101(00)00099-4
  10. Colin, S. P. & Dam, H. G. 2003. Effects of the toxic dinoflagellate Alexandrium fundyense on the copepod Acartia hudsonica: a test of the mechanisms that reduce ingestion rates. Mar. Ecol. Prog. Ser. 248:55-65. https://doi.org/10.3354/meps248055
  11. Cram, D. L. & Schulein, F. H. 1974. Observations on surface-shoaling Cape hake off South West Africa. ICES J. Mar. Sci. 35:272-275. https://doi.org/10.1093/icesjms/35.3.272
  12. Cusick, K. D. & Widder, E. A. 2014. Intensity differences in bioluminescent dinoflagellates impact foraging efficiency in a nocturnal predator. Bull. Mar. Sci. 90:797-811. https://doi.org/10.5343/bms.2013.1059
  13. Cusick, K. D. & Widder, E. A. 2020. Bioluminescence and toxicity as driving factors in harmful algal blooms: ecological functions and genetic variability. Harmful Algae 98:101850. https://doi.org/10.1016/j.hal.2020.101850
  14. Cussatlegras, A. -S. & Le Gal, P. 2007. Variability in the bioluminescence response of the dinoflagellate Pyrocystis lunula. J. Exp. Mar. Biol. Ecol. 343:74-81. https://doi.org/10.1016/j.jembe.2006.11.009
  15. Daugbjerg, N., Hansen, G., Larsen, J. & Moestrup, O. 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 39:302-317. https://doi.org/10.2216/i0031-8884-39-4-302.1
  16. Draisci, R., Ferretti, E., Palleschi, L., Marchiafava, C., Poletti, R., Milandri, A., Ceredi, A. & Pompei, M. 1999. High levels of yessotoxin in mussels and presence of yessotoxin and homoyessotoxin in dinoflagellates of the Adriatic Sea. Toxicon 37:1187-1193. https://doi.org/10.1016/S0041-0101(98)00254-2
  17. Dunn, O. J. 1961. Multiple comparisons among means. J. Am. Stat. Assoc. 56:52-64. https://doi.org/10.1080/01621459.1961.10482090
  18. Eckert, R. 2015. Excitation and luminescence in Noctiluca miliaris. In Johnson, F. H. & Haneda, Y. (Eds.) Bioluminescence in Progress. Princeton University Press, Princeton, NJ, pp. 269-300.
  19. Eckford-Soper, L. K., Bresnan, E., Lacaze, J. -P., Green, D. H. & Davidson, K. 2016. The competitive dynamics of toxic Alexandrium fundyense and non-toxic Alexandrium tamarense: the role of temperature. Harmful Algae 53:135-144. https://doi.org/10.1016/j.hal.2015.11.010
  20. Esaias, W. E. & Curl, H. C. Jr. 1972. Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limnol. Oceanogr. 17:901-906. https://doi.org/10.4319/lo.1972.17.6.0901
  21. Esaias, W. E., Curl, H. C. Jr. & Seliger, H. H. 1973. Action spectrum for a low intensity, rapid photoinhibition of mechanically stimulable bioluminescence in the marine dinoflagellates Gonyaulax catenella, G. acatenella, and G. tamarensis. J. Cell. Physiol. 82:363-372. https://doi.org/10.1002/jcp.1040820306
  22. Fogel, M. & Hastings, J. W. 1972. Bioluminescence: mechanism and mode of control of scintillon activity. Proc. Natl. Acad. Sci. U. S. A. 69:690-693. https://doi.org/10.1073/pnas.69.3.690
  23. Games, P. A. & Howell, J. F. 1976. Pairwise multiple comparison procedures with unequal n's and/or variances: a Monte Carlo study. J. Educ. Stat. 1:113-125. https://doi.org/10.2307/1164979
  24. Gu, H. 2011. Morphology, phylogenetic position, and ecophysiology of Alexandrium ostenfeldii (Dinophyceae) from the Bohai Sea, China. J. Syst. Evol. 49:606-616. https://doi.org/10.1111/j.1759-6831.2011.00160.x
  25. Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234-236. https://doi.org/10.2216/i0031-8884-32-3-234.1
  26. Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8:229-239. https://doi.org/10.1139/m62-029
  27. Guiry, M. D. & Guiry, G. M. 2021. AlgaeBase. Available from: https://www.algaebase.org. Accessed Oct 10, 2021.
  28. Haddock, S. H. D., Moline, M. A. & Case, J. F. 2010. Bioluminescence in the sea. Annu. Rev. Mar. Sci. 2:443-493. https://doi.org/10.1146/annurev-marine-120308-081028
  29. Hastings, J. W. & Sweeney, B. M. 1957. The luminescent reaction in extracts of the marine dinoflagellate, Gonyaulax polyedra. J. Cell. Comp. Physiol. 49:209-225. https://doi.org/10.1002/jcp.1030490205
  30. Higman, W. A., Stone, D. M. & Lewis, J. M. 2001. Sequence comparisons of toxic and non-toxic Alexandrium tamarense (Dinophyceae) isolates from UK waters. Phycologia 40:256-262. https://doi.org/10.2216/i0031-8884-40-3-256.1
  31. Huelsenbeck, J. P. & Ronquist, F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. https://doi.org/10.1093/bioinformatics/17.8.754
  32. Jacobson, D. M. & Anderson, D. M. 1996. Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol. 32:279-285. https://doi.org/10.1111/j.0022-3646.1996.00279.x
  33. Jang, S. H. & Jeong, H. J. 2020. Spatio-temporal distributions of the newly described mixotrophic dinoflagellate Yihiella yeosuensis (Suessiaceae) in Korean coastal waters and its grazing impact on prey populations. Algae 35:45-59. https://doi.org/10.4490/algae.2020.35.2.24
  34. Jeong, H. J., Kang, H. C., Lim, A. S., Jang, S. H., Lee, K., Lee, S. Y., Ok, J. H., You, J. H., Kim, J. H., Lee, K. H., Park, S. A., Eom, S. H., Yoo, Y. D. & Kim, K. Y. 2021. Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance. Sci. Adv. 7:eabe4214. https://doi.org/10.1126/sciadv.abe4214
  35. Jeong, H. J., Lim, A. S., Franks, P. J. S., Lee, K. H., Kim, J. H., Kang, N. S., Lee, M. J., Jang, S. H., Lee, S. Y., Yoon, E. Y., Park, J. Y., Yoo, Y. D., Seong, K. A., Kwon, J. E. & Jang, T. Y. 2015. A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97-115. https://doi.org/10.1016/j.hal.2015.06.004
  36. Jeong, H. J., Lim, A. S., Lee, K., Lee, M. J., Seong, K. A., Kang, N. S., Jang, S. H., Lee, K. H., Lee, S. Y., Kim, M. O., Kim, J. H., Kwon, J. E., Kang, H. C., Kim, J. S., Yuh, W., Shin, K., Jang, P. K., Ryu, J. -H., Kim, S. Y., Park, J. Y. & Kim, K. Y. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. Temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae 32:101-130. https://doi.org/10.4490/algae.2017.32.5.30
  37. Jeong, H. J., Park, J. Y., Nho, J. H., Park, M. O., Ha, J. H., Seong, K. A., Jeng, C., Seong, C. N., Lee, K. Y. & Yih, W. H. 2005. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol. 41:131-143. https://doi.org/10.3354/ame041131
  38. John, U., Litaker, R. W., Montresor, M., Murray, S., Brosnahan, M. L. & Anderson, D. M. 2014. Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165:779-804. https://doi.org/10.1016/j.protis.2014.10.001
  39. Kang, H. C., Jeong, H. J., Kim, S. J., You, J. H. & Ok, J. H. 2018. Differential feeding by common heterotrophic protists on 12 different Alexandrium species. Harmful Algae 78:106-117. https://doi.org/10.1016/j.hal.2018.08.005
  40. Kang, H. C., Jeong, H. J., Ok, J. H., You, J. H., Jang, S. H., Lee, S. Y., Lee, K. H., Park, J. Y. & Rho, J. -R. 2019. Spatial and seasonal distributions of the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) in Korea: quantification using qPCR. Algae 34:111-126. https://doi.org/10.4490/algae.2019.34.5.25
  41. Kelly, M. G. 1968. The occurrence of dinoflagellate luminescence at Woods Hole. Biol. Bull. 135:279-295. https://doi.org/10.2307/1539782
  42. Krasnow, R., Dunlap, J. C., Taylor, W., Hastings, J. W., Vetterling, W. & Gooch, V. 1980. Circadian spontaneous bioluminescent glow and flashing of Gonyau1ax polyedra. J. Comp. Phvsiol. 138:19-26. https://doi.org/10.1007/BF00688730
  43. Kremp, A., Lindholm, T., Dressler, N., Erler, K., Gerdts, G., Eirtovaara, S. & Leskinen, E. 2009. Bloom forming Alexandrium ostenfeldii (Dinophyceae) in shallow waters of the Aland archipelago, Northern Baltic Sea. Harmful Algae 8:318-328. https://doi.org/10.1016/j.hal.2008.07.004
  44. Kruskal, W. H. & Wallis, W. A. 1952. Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47:583-621 https://doi.org/10.1080/01621459.1952.10483441
  45. Laabir, M., Jauzein, C., Genovesi, B., Masseret, E., Grzebyk, D., Cecchi, P., Vaquer, A., Perrin, Y. & Collos, Y. 2011. Influence of temperature, salinity and irradiance on the growth and cell yield of the harmful red tide dinoflagellate Alexandrium catenella colonizing Mediterranean waters. J. Plankton Res. 33:1550-1563. https://doi.org/10.1093/plankt/fbr050
  46. Lapota, D., Geiger, M. L., Stiffey, A. V., Rosenberger, D. E. & Young, D. K. 1989. Correlations of planktonic bioluminescence with other oceanographic parameters from a Norwegian fjord. Mar. Ecol. Prog. Ser. 55:217-227. https://doi.org/10.3354/meps055217
  47. Latz, M. I., Bovard, M., VanDelinder, V., Segre, E., Rohr, J. & Groisman, A. 2008. Bioluminescent response of individual dinoflagellate cells to hydrodynamic stress measured with millisecond resolution in a microfluidic device. J. Exp. Biol. 211:2865-2875. https://doi.org/10.1242/jeb.011890
  48. Latz, M. I. & Jeong, H. J. 1996. Effect of red tide dinoflagellate diet and cannibalism on the bioluminescence of the heterotrophic dinoflagellates Protoperidinium spp. Mar. Ecol. Prog. Ser. 132:275-285. https://doi.org/10.3354/meps132275
  49. Latz, M. I. & Lee, A. O. 1995. Spontaneous and stimulated bioluminescence of the dinoflagellate Ceratocorys horrzda (Peridiniales). J. Phycol. 31:120-132. https://doi.org/10.1111/j.0022-3646.1995.00120.x
  50. Latz, M. I., Nauen, J. C. & Rohr, J. 2004. Bioluminescence response of four species of dinoflagellates to fully developed pipe flow. J. Plankton Res. 26:1529-1546. https://doi.org/10.1093/plankt/fbh141
  51. Le Tortorec, A. H., Tahvanainen, P., Kremp, A. & Simis, S. G. H. 2016. Diversity of luciferase sequences and bioluminescence production in Baltic Sea Alexandrium ostenfeldii. Eur. J. Phycol. 51:317-327. https://doi.org/10.1080/09670262.2016.1160441
  52. Lee, K. H., Jeong, H. J., Kang, H. C., Ok, J. H., You, J. H. & Park, S. A. 2019. Growth rates and nitrate uptake of co-occurring red-tide dinoflagellates Alexandrium affine and A. fraterculus as a function of nitrate concentration under light-dark and continuous light conditions. Algae 34:237-251. https://doi.org/10.4490/algae.2019.34.8.28
  53. Lee, K. H., Jeong, H. J., Kwon, J. E., Kang, H. C., Kim, J. H., Jang, S. H., Park, J.Y., Yoon, E. Y. & Kim, J. S. 2016. Mixotrophic ability of the phototrophic dinoflagellates Alexandrium andersonii, A. affine, and A. fraterculus. Harmful Algae 59:67-81. https://doi.org/10.1016/j.hal.2016.09.008
  54. Lee, S. Y., Jeong, H. J., Ok, J. H., Kang, H. C. & You, J. H. 2020. Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters. Algae 35:225-236. https://doi.org/10.4490/algae.2020.35.8.25
  55. Lewis, N. I., Xu, W., Jericho, S. K., Kreuzer, H. J., Jericho, M. H. & Cembella, A. D. 2006. Swimming speed of three species of Alexandrium (Dinophyceae) as determined by digital in-line holography. Phycologia 45:61-70. https://doi.org/10.2216/04-59.1
  56. Lilly, E. L., Halanych, K. M. & Anderson, D. M. 2005. Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae 4:1004-1020. https://doi.org/10.1016/j.hal.2005.02.001
  57. Lim, A. S., Jeong, H. J., Kim, J. H., Jang, S. H., Lee, M. J. & Lee, K. 2015. Mixotrophy in the newly described dinoflagellate Alexandrium pohangense: a specialist for feeding on the fast-swimming ichthyotoxic dinoflagellate Cochlodinium polykrikoides. Harmful Algae 49:10-18. https://doi.org/10.1016/j.hal.2015.07.010
  58. Lim, A. S., Jeong, H. J. & Ok, J. H. 2019. Five Alexandrium species lacking mixotrophic ability. Algae 34:289-301. https://doi.org/10.4490/algae.2019.34.11.21
  59. Lim, A. S., Jeong, H. J., Ok, J. H. & Kim, S. J. 2018. Feeding by the harmful phototrophic dinoflagellate Takayama tasmanica (Family Kareniaceae). Harmful Algae 74:19-29. https://doi.org/10.1016/j.hal.2018.03.009
  60. Lindstrom, J., Grebner, W., Rigby, K. & Selander, E. 2017. Effects of predator lipids on dinoflagellate defense mechanisms-increased bioluminescence capacity. Sci. Rep. 7:13104. https://doi.org/10.1038/s41598-017-13293-4
  61. 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 organisms using internal transcribed spacer-specific PCR assays. J. Phycol. 39:754-761. https://doi.org/10.1046/j.1529-8817.2003.02112.x
  62. Liu, L., Wilson, T. & Hastings, J. W. 2004. Molecular evolution of dinoflagellate luciferases, enzymes with three catalytic domains in a single polypeptide. Proc. Natl. Acad. Sci. U. S. A. 101:16555-16560. https://doi.org/10.1073/pnas.0407597101
  63. MacKenzie, L., de Salas, M., Adamson, J. & Beuzenberg, V. 2004. The dinoflagellate genus Alexandrium (Halim) in New Zealand coastal waters: comparative morphology, toxicity and molecular genetics. Harmful Algae 3:71-92. https://doi.org/10.1016/j.hal.2003.09.001
  64. Mann, H. B. & Whitney, D. R. 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18:50-60. https://doi.org/10.1214/aoms/1177730491
  65. Marcinko, C. L. J., Painter, S. C., Martin, A. P. & Allen, J. T. 2013. A review of the measurement and modelling of dinoflagellate bioluminescence. Prog. Oceanogr. 109:117-129. https://doi.org/10.1016/j.pocean.2012.10.008
  66. Martinez, A., Mendez, S. & Fabre, A. 2016. First record of bioluminescence of Alexandrium fraterculus (dinoflagellate), in the Uruguayan coast, South Western Atlantic Ocean. Pan-Am. J. Aquat. Sci. 11:356-360.
  67. McCapra, F. 1976. Chemical mechanisms in bioluminescence. Acc. Chem. Res. 9:201-208. https://doi.org/10.1021/ar50102a001
  68. Miller, S. D., Haddock, S. H. D., Elvidge, C. D. & Lee, T. F. 2005. Detection of a bioluminescent milky sea from space. Proc. Natl. Acad. Sci. U. S. A. 102:14181-14184. https://doi.org/10.1073/pnas.0507253102
  69. Montresor, M., John, U., Beran, A. & Medlin, L. K. 2004. Alexandrium tamutum sp. nov. (Dinophyceae): a new nontoxic species in the genus Alexandrium. J. Phycol. 40:398-411. https://doi.org/10.1111/j.1529-8817.2004.03060.x
  70. Murakami, M., Makabe, K., Yamaguchi, K., Konosu, S. & Walchli, M. R. 1988. Goniodomin A, a novel polyether macrolide from the dinoflagellate Goniodoma pseudogoniaulax. Tetrahedron Lett. 29:1149-1152. https://doi.org/10.1016/S0040-4039(00)86674-5
  71. Murakami, M., Okita, Y., Matsuda, H., Okino, T. & Yamaguchi, K. 1998. From the dinoflagellate Alexandrium hiranoi. Phytochemistry 48:85-88. https://doi.org/10.1016/S0031-9422(97)00756-5
  72. Murray, S., John, U., Savela, H. & Kremp, A. 2020. Alexandrium spp.: genetic and ecological factors influencing saxitoxin production and proliferation. In Botana, L. M., Louzao, M. C. & Vilarino, N. (Eds.) Climate Change and Marine and Freshwater Toxins. Walter de Gruyter, Berlin, pp. 133-166.
  73. Nguyen-Ngoc, L. 2004. An autecological study of the potentially toxic dinoflagellate Alexandrium affine isolated from Vietnamese waters. Harmful Algae 3:117-129. https://doi.org/10.1016/S1568-9883(03)00062-3
  74. Orr, R. J. S., Stuken, A., Murray, S. A. & Jakobsen, K. S. 2013. Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: the second "core" gene, sxtG. Appl. Environ. Microbiol. 79:2128-2136. https://doi.org/10.1128/AEM.03279-12
  75. Orr, R. J. S., Stuken, A., Rundberget, T., Eikrem, W. & Jakobsen, K. S. 2011. Improved phylogenetic resolution of toxic and non-toxic Alexandrium strains using a concatenated rDNA approach. Harmful Algae 10:676-688. https://doi.org/10.1016/j.hal.2011.05.003
  76. Prakash, A. & Taylor, F. J. R. 1966. A "red water" bloom of Gonyaulax acatenella in the Strait of Georgia and its relation to paralytic shellfish toxicity. J. Fish. Res. Board Can. 23:1265-1270. https://doi.org/10.1139/f66-115
  77. Rohr, J., Latz, M. I., Fallon, S., Nauen, J. C. & Hendricks, E. 1998. Experimental approaches towards interpreting dolphin-stimulated bioluminescence. J. Exp. Biol. 201:1447-1460. https://doi.org/10.1242/jeb.201.9.1447
  78. Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. https://doi.org/10.1093/bioinformatics/btg180
  79. Satake, M., MacKenzie, L. & Yasumoto, T. 1997. Identification of Protoceratium reticulatum as the biogenetic origin of yessotoxin. Nat. Toxins 5:164-167. https://doi.org/10.1002/19970504NT7
  80. Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. 1994. Identification of group- and strain-specific genetic makers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30:999-1011. https://doi.org/10.1111/j.0022-3646.1994.00999.x
  81. Seliger, H. H., Biggley, W. H. & Swift, E. 1969. Absolute values of photon emission from the marine dinoflagellates Pyrodinium bahamense, Gonyaulax polyedra and Pyrocystis lunula. Photochem. Photobiol. 10:227-232. https://doi.org/10.1111/j.1751-1097.1969.tb05685.x
  82. Shimomura, O. 2006. Bioluminescence: chemical principles and methods. World Scientific, Toh Tuck Link, 500 pp.
  83. Stamatakis, A. 2006. RaxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  84. Subong, B. J. J., Benico, G. A., Sulit, A. K. L., Mendoza, C. O., Cruz, L. J., Azanza, R. V. & Jimenez, E. C. 2017. Toxicity and protein expression of Alexandrium species collected in the Philippine waters. Philipp. J. Sci. 146:425-436.
  85. Sullivan, J. M. & Swift, E. 1995. Photoenhancement of bioluminescence capacity in natural and laboratory populations of the autotrophic dinoflagellate Ceratium fusus (Ehrenb.) Dujardin. J. Geophys. Res. Oceans 100: 6565-6574. https://doi.org/10.1029/94JC01511
  86. Sweeney, B. M. 1963. Bioluminescent dinoflagellates. Biol. Bull. 125:177-181. https://doi.org/10.2307/1539300
  87. Sweeney, B. M. 1986. The loss of the circadian rhythm in photosynthesis in an old strain of Gonyaulax polyedra. Plant Physiol. 80:978-981. https://doi.org/10.1104/pp.80.4.978
  88. Swift, E., Biggley, W. H. & Seliger, H. H. 1973. Species of oceanic dinoflagellates in the genera Dissodinium and Pyrocystis: interclonal and interspecific comparisons of the color and photon yield of bioluminescence. J. Phycol. 9:420-426. https://doi.org/10.1111/j.1529-8817.1973.tb04115.x
  89. Swift, E., Sullivan, J. M., Batchelder, H. P., Van Keuren, J., Vaillancourt, R. D. & Bidigare, R. R. 1995. Bioluminescent organisms and bioluminescence measurements in the North Atlantic Ocean near latitude 59.5°N, longitude 21°W. J. Geophys. Res. Oceans 100:6527-6547. https://doi.org/10.1029/94JC01870
  90. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599. https://doi.org/10.1093/molbev/msm092
  91. Valiadi, M. & Iglesias-Rodriguez, D. 2013. Understanding bioluminescence in dinoflagellates: how far have we come? Microorganisms 1:3-25. https://doi.org/10.3390/microorganisms1010003
  92. Valiadi, M., Iglesias-Rodriguez, M. D. & Amorim, A. 2012. Distribution and genetic diversity of the luciferase gene within marine dinoflagellates. J. Phycol. 48:826-836. https://doi.org/10.1111/j.1529-8817.2012.01144.x
  93. Von Dassow, P. & Latz, M. I. 2002. The role of Ca2+ in stimulated bioluminescence of the dinoflagellate Lingulodinium polyedrum. J. Exp. Biol. 205:2971-2986. https://doi.org/10.1242/jeb.205.19.2971
  94. Welch, B. L. 1947. The generalization of 'student's' problem when several different population variances are involved. Biometrika 34:28-35. https://doi.org/10.1093/biomet/34.1-2.28
  95. White, H. H. 1979. Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J. Exp. Mar. Biol. Ecol. 36:217-224. https://doi.org/10.1016/0022-0981(79)90117-5
  96. Widder, E. A. 2010. Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328:704-708. https://doi.org/10.1126/science.1174269
  97. Widder, E. A. & Case, J. F. 1981. Two flash forms in the bioluminescent dinoflagellate, Pyrocystis fusiformis. J. Comp. Physiol. 143:43-52. https://doi.org/10.1007/BF00606067
  98. Wilson, T. & Hastings, J. W. 2013. Bioluminescence: living lights, lights for living. Harvard University Press, Cambridge, MA, 185 pp.
  99. Wohlrab, S., Iversen, M. H. & John, U. 2010. A molecular and co-evolutionary context for grazer induced toxin production in Alexandrium tamarense. PLoS ONE 5:e15039. https://doi.org/10.1371/journal.pone.0015039
  100. Yoo, Y. D., Jeong, H. J., Kim, M. S., Kang, N. S., Song, J. Y., Shin, W., Kim, K. Y. & Lee, K. 2009. Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 56:413-420. https://doi.org/10.1111/j.1550-7408.2009.00421.x