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Dinoflagellata

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Abstract

Dinoflagellates are a major group of aquatic protists responsible for a major part of marine primary productivity, the creation of coral reefs, marine bioluminescence, and most toxic red tides; indirectly they also cause some human diseases like paralytic shellfish poisoning, ciguatera, etc. They are derived from photosynthetic ancestors and early in their evolutionary history exchanged most of the histones in their nuclei for DVNPs, proteins of putatively viral origin that caused a complete reorganization of chromosomes that includes the loss of the typical eukaryotic nucleosomes and a very marked increase in total amounts of DNA per nucleus. Later on, they acquired other types of DNA-binding proteins, so-called HLPs in at least two waves, possibly lateral transfers from bacteria. Dinoflagellate mitochondrial genomes are some of the smallest known, and the genomes of the ancestral plastid type of the group, the peridinin plastids, are atomized into mini-circles with usually one single gene per circle. Roughly half of the dinoflagellates are non-photosynthetic, and the majority of the photosynthetic forms have peridinin plastids. Loss of photosynthesis has occurred repeatedly, but all free-living non-photosynthetic forms remain metabolically dependent on cryptic plastids; complete loss of plastid metabolic activity has only been shown in a few parasitic forms. Several lineages show a marked propensity for reacquisition of photosynthesis, be it in the form of permanent photosynthetic endosymbionts, kleptochloroplasts, or serial secondary and tertiary endosymbioses that produce cells with a wide variety of plastid types. In a few members of the group, peridinin plastids have become the pigment cup/retinoid of complex eyelike structures, so-called ocelli.

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References

  • Akimoto, H., Wu, C., Kinumi, T., & Ohmiya, Y. (2004). Biological rhythmicity in expressed proteins of the marine dinoflagellate L. polyedrum demonstrated by chronological proteomics. Biochemical and Biophysical Research Communications, 315, 306–312.

    Article  CAS  PubMed  Google Scholar 

  • Alam, M., Sansing, T. B., Busby, E. L., Martiniz, D. R., & Ray, S. M. (1979). Dinoflagellate sterols I: Sterol composition of the dinoflagellates of Gonyaulax species. Steroids, 33, 197–203.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, D. M., & Lobel, P. S. (1987). The continuing enigma of ciguatera. Biological Bulletin, 172, 89–107.

    Article  CAS  Google Scholar 

  • Anderson, D. M., & Stolzenbach, K. D. (1985). Selective retention of two dinoflagellates in a well-mixed estuarine embayment: The importance of diel migration and surface avoidance. Marine Ecology Progress Series, 25, 39–50.

    Article  Google Scholar 

  • Bachvaroff, T. R., & Place, A. R. (2008). From stop to start: Tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PloS ONE, 3, e2929.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bachvaroff, T. R., Concepción, G. T., Rogers, C. R., Herman, E. M., & Delwiche, C. F. (2004). Dinoflagellate expressed sequence tag data indicate massive transfer of chloroplast genes to the nuclear genome. Protist, 155, 65–78.

    Article  CAS  PubMed  Google Scholar 

  • Bachvaroff, T. R., Gornik, S. G., Concepcion, G. T., Waller, R. F., Mendez, G. S., Lippmeier, J. C., & Delwiche, C. F. (2014). Dinoflagellate phylogeny revisited: Using ribosomal proteins to resolve deep branching dinoflagellate clades. Molecular Phylogenetics and Evolution, 70, 314–322.

    Article  CAS  PubMed  Google Scholar 

  • Banaszak, A., Iglesias-Prieto, R., & Trench, R. K. (1993). Scrippsiella velellae sp. nov. (Peridiniales) and Gloeodinium viscum sp. nov. (Phytodiniales), dinoflagellate symbionts of two hydrozoans (Cnidaria). Journal of Phycology, 29, 517–528.

    Article  Google Scholar 

  • Bouck, G. B., & Sweeney, B. M. (1966). The fine structure and ontogeny of trichocysts in marine dinoflagellates. Protoplasma, 61, 205–223.

    Article  CAS  PubMed  Google Scholar 

  • Brate, J., Krabberød, A. K., Dolven, J. K., Ose, R. F., Kristensen, T., Bjørklund, K. R., & Shalchian-Tabrizi, K. (2012). Radiolaria associated with a large diversity of marine alveolates. Protist, 163, 767–777.

    Article  PubMed  Google Scholar 

  • Buskey, E. J., & Swift, E. (1983). Behavioral responses of the coastal copepod Acartia hudsonica (Pinhey) to simulated dinoflagellate bioluminescence. Journal of Experimental Marine Biology and Ecology, 72, 43–58.

    Article  Google Scholar 

  • Cachon, J., & Cachon, M. (1987). Parasitic dinoflagellates, Chapter 13. In F. J. R. Taylor (Ed.), The biology of dinoflagellates (pp. 571–610). Oxford: Blackwell.

    Google Scholar 

  • Cavalier-Smith, T. (1991). Cell diversification in heterotrophic flagellates. In D. J. Patterson & J. Larsen (Eds.), The biology of free-living heterotrophic flagellates (The Systematics Association special volume, Vol. 45). Oxford: Clarendon Press.

    Google Scholar 

  • Cavalier-Smith, T., & Chao, E. E. (2004). Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates. European Journal of Protistology, 40, 185–212.

    Article  Google Scholar 

  • Cembella, A. D. (2003). Chemical ecology of eukaryotic microalgae in marine ecosystems. Phycologia, 42, 420–447.

    Article  Google Scholar 

  • Coats, D. W., Bachvaroff, T. R., & Delwiche, C. F. (2012). Revision of the family Duboscquellidae with description of Euduboscquella crenulata n. gen., n. sp. (Dinoflagellata, Syndinea), an intracellular parasite of the ciliate Favella panamensis Kofoid & Campbell, 1929. Journal of Eukaryotic Microbiology, 59, 1–11.

    Article  PubMed  Google Scholar 

  • Coffroth, M. A., & Santos, S. R. (2005). Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist, 156, 19–34.

    Article  CAS  PubMed  Google Scholar 

  • Cullen, J. J., & MacIntyre, J. G. (1998). Behavior, physiology and the niche of depth-regulating phytoplankton. In D. M. Anderson, A. D. Cembella, & G. M. Hallegraeff (Eds.), Physiological ecology of harmful algal blooms (pp. 559–580). Berlin: Springer.

    Google Scholar 

  • Dale, B. (1983). Dinoflagellate resting cysts: “benthic plankton”. In G. A. Fryxell (Ed.), Survival strategies of the algae (pp. 69–136). Cambridge: Cambridge University Press.

    Google Scholar 

  • 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, 302–317.

    Article  Google Scholar 

  • Daugbjerg, N., Hastrup Jensen, M., & Hansen, P. J. (2013). Using nuclear-encoded LSU and SSU rDNA sequences to identify the eukaryotic endosymbiont in Amphisolenia bidentata (Dinophyceae). Protist, 164, 411–422.

    Article  CAS  PubMed  Google Scholar 

  • De Vargas, C., Audic, S., Henry, N., Decelle, J., Mahé, F., Logares, R., Lara, E., Berney, C., Le Bescot, N., Probert, I., et al. (2015). Eukaryotic plankton diversity in the sunlit ocean. Science, 348(6237), 1261605.

    Article  PubMed  CAS  Google Scholar 

  • Dodge, J. D. (1965). Chromosome structure in the dinoflagellates and the problem of mesokaryotic cells. Excerpta Medica International Congress Series, 91, 339–345.

    Google Scholar 

  • Dodge, J. D. (1966). The dinophyceae. In M. B. E. Godward (Ed.), The chromosomes of the algae (pp. 96–115). New York: St. Martin’s Press.

    Google Scholar 

  • Dodge, J. D. (1973). The fine structure of algal cells. London: Academic.

    Google Scholar 

  • Dodge, J. D. (1982). Marine dinoflagellates of the British Isles. London: Her Majesty’s Stationary Office.

    Google Scholar 

  • Dodge, J. D. (1987). Dinoflagellate ultrastructure. In F. J. R. Taylor (Ed.), The biology of dinoflagellates (Botanical monographs, Vol. 21). Oxford: Blackwell.

    Google Scholar 

  • Dolven, J. K., Lindqvist, C., Albert, V. A., Bjørklund, K. R., Yuasa, T., Takahashi, O. & Mayama, S. (2007). Molecular diversity of alveolates associated with neritic North Atlantic radiolarians. Protist, 158, 65–76.

    Article  CAS  PubMed  Google Scholar 

  • Evitt, W. R. (1985). Sporopollenin dinoflagellate cysts: Their morphology and interpretation. American Association Stratigraphic Palynologists Monograph Ser. 1.

    Google Scholar 

  • Fast, N. M., Kissinger, J. C., Roos, D. S., & Keeling, P. J. (2001). Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Molecular Biology and Evolution, 18, 418–426.

    Article  CAS  PubMed  Google Scholar 

  • Fast, N. M., Xue, L., Bingham, S., & Keeling, P. J. (2002). Re-examining alveolate evolution using multiple protein molecular phylogenies. Journal of Eukaryotic Microbiology, 49, 30–37.

    Article  CAS  PubMed  Google Scholar 

  • Fensome R. A., Taylor, F. J. R., Norris, G., Sarjeant, W. A. S., Wharton, D. I., & Williams, G. L. (1993). A classification of living and fossil dinoflagellates (Micropaleontology special publication, Vol. 7). Hanover: Sheridan Press.

    Google Scholar 

  • Fensome, R. A., Saldarriaga, J. F., & Taylor, F. J. R. (1999). Dinoflagellate phylogeny revisited: Reconciling morphological and molecular based phylogenies. Grana, 38, 66–80.

    Article  Google Scholar 

  • Fernández Robledo, J. A., Caler, E., Matsuzaki, M., Keeling, P. J., Shanmugam, D., Roos, D. S., & Vasta, G. R. (2011). The search for the missing link: A relic plastid in Perkinsus? International Journal for Parasitology, 41, 1217–1229.

    Article  PubMed  CAS  Google Scholar 

  • Fleischer, K., & Case, J. F. (1995). Cephalopod predation facilitated by dinoflagellate luminescence. Biological Bulletin, 189, 263–271.

    Article  Google Scholar 

  • Flø-Jørgensen, M., Murray, S., & Daugbjerg, N. (2004). Amphidinium revisited. I. Redefinition of Amphidinium (Dinophyceae) based on cladistic and molecular phylogenetic analyses. Journal of Phycology, 40, 351–365.

    Article  Google Scholar 

  • Gaines, G., & Elbrächter, M. (1987) Heterotrophic nutrition. In F. J. R. Taylor (Ed.), The biology of dinoflagellates (Botanical monographs, Vol. 21). Oxford: Blackwell.

    Google Scholar 

  • Gaines, G., & Taylor, F. J. R. (1984). Extracellular digestion in marine dinoflagellates. Journal of Plankton Research, 6, 1057–1061.

    Article  Google Scholar 

  • Gaines, G., & Taylor, F. J. R. (1985). Form and function of the dinoflagellate transverse flagellum. Journal of Protozoology, 32, 290–296.

    Article  Google Scholar 

  • Gavelis, G. S., Hayakawa, S., White III, R. A., Gojoburi, T., Suttle, C. A., Keeling, P. J., & Leander, B. S. (2015). Eye-like ocelloids are built from different endosymbiotically acquired components. Nature, 523, 204–207.

    Article  CAS  PubMed  Google Scholar 

  • Gawryluk, R. M. R., del Campo, J., Okamoto, N., Strassert, J. F. H., Lukeš, J., Richards, T. A., Worden, A. Z., Santoro, A. E., & Keeling, P. J. (2016). Morphological identification and single-cell genomics of marine diplonemids. Current Biology, 26, 3053–3059.

    Article  CAS  PubMed  Google Scholar 

  • Gómez, F. (2003). Checklist of Mediterranean free-living dinoflagellates. Botanica Marina, 46, 215–242.

    Article  Google Scholar 

  • Gómez, F. (2005). A list of dinoflagellates in the world oceans. Acta Botanica Croatica, 64, 129–212.

    Google Scholar 

  • Gómez, F. (2012). A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Systematics and Biodiversity, 10, 267–275.

    Article  Google Scholar 

  • Gómez, F., & Furuya, K. (2007). Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology, 43, 115–124.

    Article  PubMed  Google Scholar 

  • Gornik, S., Ford, K. L., Mulhern, T. D., Bacic, A., McFadden, G. I., & Waller, R. F. (2012). Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Current Biology, 22, 2303–2312.

    Article  CAS  PubMed  Google Scholar 

  • Gornik, S., Febrimarsa, Cassin, A. M., MacRae, J. I., Ramaprasad, A., Rchiad, Z., McConville, M. J., Bacic, A., McFadden, G. I., Pain, A., & Waller, R. F. (2015). Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proceedings of the National Academy of Sciences of the United States of America, 112, 5767–5772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Granéli, E., & Turner, J. T. (2006). Ecology of harmful algae (Ecological studies, Vol. 189). Berlin: Springer.

    Google Scholar 

  • Green, B. R. (2004). The chloroplast genome of dinoflagellates: A reduced instruction set? Protist, 155, 23–31.

    Article  CAS  PubMed  Google Scholar 

  • Greuet, C. (1978). Ultrastructural organization of the ocelloid of Nematodinium. Phylogenetic aspect of the evolution of Warnowiidae Lindemann dinoflagellates photoreceptor. Cytobiology, 17, 114–136.

    CAS  Google Scholar 

  • Guillard, R. L., & Keller, M. D. (1984). Culturing dinoflagellates. In D. L. Spector (Ed.), Dinoflagellates (pp. 391–442). New York: Academic.

    Chapter  Google Scholar 

  • Hackett, J. D., Yoon, H. S., Soares, M. B., Bonaldo, M. F., Casavant, T., Scheetz, T. E., Nosenko, T., & Bhattacharya, D. (2004a). Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Current Biology, 14, 213–218.

    Article  CAS  PubMed  Google Scholar 

  • Hackett, J. D., Anderson, D. M., Erdner, D. L., & Bhattacharya, D. (2004b). Dinoflagellates: A remarkable evolutionary experiment. American Journal of Botany, 91, 1523–1534.

    Article  CAS  PubMed  Google Scholar 

  • Hansen, G., & Daugbjerg, N. (2004). Ultrastructure of Gyrodinium spirale, the type species of Gyrodinium (Dinophyceae) including a phylogeny of G. dominans, G. rubrum and G. spirale deduced from partial LSU rDNA sequences. Protist, 155, 271–294.

    Article  CAS  PubMed  Google Scholar 

  • Hansen, G., Daugbjerg, N., & Henriksen, P. (2007). Baldinia anauniensis gen. et sp. nov.: A ‘new’ dinoflagellate from Lake Tovel, N. Italy. Phycologia, 46, 86–108.

    Article  Google Scholar 

  • Harada, A., Ohtsuka, S., & Horiguchi, T. (2007). Species of the parasitic genus Duboscquella are members of the enigmatic marine alveolate group 1. Protist, 158, 337–347.

    Article  CAS  PubMed  Google Scholar 

  • Harper, J. T., & Keeling, P. J. (2003). Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromist and alveolate plastids. Molecular Biology and Evolution, 20, 1730–1735.

    Article  CAS  PubMed  Google Scholar 

  • Hastings, J. W. (1986). Bioluminescence in bacteria and dinoflagellates. In Govindjee, D. Fork, & J. Amesz (Eds.), Luminescence in plants. New York: Academic.

    Google Scholar 

  • Hastings, J. W. (1996). Chemistries and colours of bioluminescent reactions: A review. Gene, 173, 5–11.

    Article  CAS  PubMed  Google Scholar 

  • Hastings, J. W., & Sweeney, B. M. (1964). Phased cell division in the marine dinoflagellates. In E. Zeuthen (Ed.), Synchrony in cell division and growth (pp. 307–321). New York: Interscience.

    Google Scholar 

  • Head, M. J. (1996). Modern dinoflagellate cysts and their biological affinities. In J. Jansonius & D. C. McGregor (Eds.), Palinology: Principles and applications (Vol. 3, pp. 1197–1248). Dallas: American Association of Stratigraphic Palynologists Foundation.

    Google Scholar 

  • Hoppenrath, M., & Leander, B. S. (2007). Character evolution in polykrikoid dinoflagellates. Journal of Phycology, 43, 366–377.

    Article  Google Scholar 

  • Hoppenrath, M., Chomérat, N., Horiguchi, T., Schweikert, M., Nagahama, Y., & Murray, S. (2013). Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae) - a proposal and review. Harmful Algae, 27, 1–28.

    Google Scholar 

  • Hoppenrath, M., Murray, S. A., Chomérat, N., & Horiguchi, T. (2014). Marine benthic dinoflagellates: Unveiling their worldwide biodiversity (Kleine Senckenberg-Reihe, Vol. 54). Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung.

    Google Scholar 

  • Howe, C. J., Nisbet, R. E. R., & Barbrook, A. C. (2008). The remarkable chloroplast genome of dinoflagellates. Journal of Experimental Botany, 59, 1035–1045.

    Article  CAS  PubMed  Google Scholar 

  • Ishida, K., & Green, B. R. (2002). Second- and third-hand chloroplasts in dinoflagellates: Phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. Proceedings of the National Academy of Sciences of the United States of America, 99, 9294–9299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobson, D. M., & Anderson, D. M. (1992). Ultrastructure of the feeding apparatus and myonemal system of the heterotrophic dinoflagellate Protoperidinium spinulosum. Journal of Phycology, 28, 69–82.

    Article  Google Scholar 

  • Janouškovec, J., Horák, A., Oborník, M., Lukeš, J., Keeling, P. J., & Doolittle, W. F. (2010). A common red algal origin of the apicomplexan, dinoflagellate and heterokont plastids. Proceedings of the National Academy of Sciences of the United States of America, 107, 10949–10954.

    Article  PubMed  PubMed Central  Google Scholar 

  • Janouškovec, J., Tikhonenkov, D., Burki, F., Howe, A. T., Kolísko, M., Mylnikov, A. P., & Keeling, P. J. (2015). Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proceedings of the National Academy of Sciences of the United States of America, 112, 10200–10207.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Janouškovec, J., Gavelis, G. G., Burki, F., Dinh, D., Bachvaroff, T. R., Gornik, S. G., Bright, K. J., Imanian, B., Strom, S. L., Delwiche, C. F., Waller, R. F., Fensome, R. A., Leander, B. S., Rohwer, F. L., & Saldarriaga, J. F. (2016). Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proceedings of the National Academy of Sciences of the United States of America, 114, E171–E180. doi:10.1073/pnas.1614842114.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Janson, S. (2004). Molecular evidence that plastids in the toxin-producing dinoflagellate genus Dinophysis originate from the free-living cryptophyte Teleaulax amphioxeia. Environmental Microbiology, 6, 1102–1106.

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey, S. W., Sielicki, M., & Haxo, F. T. (1975). Chloroplast pigment patterns in dinoflagellates. Journal of Phycology, 11, 374–384.

    CAS  Google Scholar 

  • Johnson, C. H., & Hastings, J. W. (1986). The elusive mechanism of the circadian clock. American Scientist, 74, 29–36.

    Google Scholar 

  • Johnson, C. H., Inoué, S., Flint, A., & Hastings, J. W. (1985). Compartmentation of algal bioluminescence: Autofluorescence of bioluminescent particles in the dinoflagellate Gonyaulax as studied with image intensified video microscopy and flow cytometry. Journal of Cell Biology, 100, 1435–1446.

    Article  CAS  PubMed  Google Scholar 

  • Kim, M., Kim, K.-Y., Nam, S.-W., Shin, W., Yih, W., & Park, M.-G. (2014). The effect of starvation on plastid number and photosynthetic performance in the kleptoplastidic dinoflagellate Amylax triacantha. The Journal of Eukaryotic Microbiology, 61, 354–363.

    Article  PubMed  Google Scholar 

  • Knaust, R., Urbig, T., Li, L., Taylor, W., & Hastings, J. W. (1998). The circadian rhythm of bioluminescence in Pyrocystis is not due to differences in the amount of luciferase: A comparative study of three bioluminescent marine dinoflagellates. Journal of Phycology, 34, 167–172.

    Article  CAS  Google Scholar 

  • Koike, K., Sekiguchi, H., Kobiyama, A., Takishita, K., Kawachi, M., Koike, K., & Ogata, T. (2005). A novel type of kleptoplastidy in Dinophysis (Dinophyceae): Presence of a haptophyte-type plastid in Dinophysis mitra. Protist, 156, 225–237.

    Article  CAS  PubMed  Google Scholar 

  • Kretschmann, J., Elbrächter, M., Zinssmeister, C., Soehner, S., Kirsch, M., Kusber, W.-H. & Gottschling, M. (2015). Taxonomic classification of the dinophyte Peridinium acuminatum Ehrenb., = Scrippsiella acuminata, comb. nov. (Thoracosphaeraceae, Peridiniales). Phytotaxa, 220, 239–256.

    Article  Google Scholar 

  • Laatsch, T., Zauner, S., Stöbe-Meier, B., Kovallik, K. V., & Maier, U. G. (2004). Plastid-derived single gene minicircles of the dinoflagellate Ceratium horridum are localized in the nucleus. Molecular Biology and Evolution, 21, 1318–1322.

    Article  CAS  PubMed  Google Scholar 

  • Leander, B. S., & Hoppenrath, M. (2008). Ultrastructure of a novel tube-forming intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata, Myzozoa). European Journal of Protistology, 44, 55–70.

    Article  PubMed  Google Scholar 

  • Lehane, L., & Lewis, R. J. (2000). Ciguatera: Recent advances, but the risk remains. International Journal of Food Microbiology, 61, 91–125.

    Article  CAS  PubMed  Google Scholar 

  • Lessard, E. J., & Swift, E. (1985). Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters measured with a dual-label radioisotope technique. Marine Biology, 87, 289–296.

    Article  Google Scholar 

  • Lidie, K. B., & Van Dolah, F. M. (2007). Spliced leader RNA-mediated trans-splicing in a dinoflagellate, Karenia brevis. Journal of Eukaryotic Microbiology, 54, 427–435.

    Article  CAS  PubMed  Google Scholar 

  • Lin, S., Zhang, H., Spencer, D. F., Norman, J. E., & Grey, M. W. (2002). Widespread and extensive editing of mitochondrial mRNAs in dinoflagellates. Journal of Molecular Biology, 320, 727–739.

    Article  CAS  PubMed  Google Scholar 

  • Livolant, F. (1982a). Dinoflagellate trichocyst ultrastructure I. The shaft. Biology of the Cell, 43, 201–210.

    Google Scholar 

  • Livolant, F. (1982b). Dinoflagellate trichocyst ultrastructure II. Existence of a sheath. Biology of the Cell, 43, 211–216.

    Google Scholar 

  • Loeblich, A. R., & Loeblich III, A. R. (1966). Index to the genera, subgenera, and sections of the Pyrrhophyta. Studies of Tropical Oceanography, Miami, 3, 1–94.

    Google Scholar 

  • Logares, R., Schalchian-Tabrizi, K., Boltovskoy, A., & Rengefors, K. (2007). Extensive dinoflagellate phylogenies indicate infrequent marine-freshwater transitions. Molecular Phylogenetics and Evolution, 45, 887–903.

    Article  CAS  PubMed  Google Scholar 

  • Lowe, C. D., Day, A., Kemp, S. J., & Montagnes, D. J. S. (2005). There are high levels of functional and genetic diversity in Oxyrrhis marina. Journal of Eukaryotic Microbiology, 52, 250–257.

    Article  CAS  PubMed  Google Scholar 

  • Lundholm, N., & Moestrup, Ø.. (2006). Biogeography of harmful algae. In E. Granéli & J. T. Turner (Eds.), Ecology of harmful algae (Ecological studies, Vol. 189). Berlin: Springer.

    Google Scholar 

  • MacRae, R. A., Fensome, R. A., & Williams, G. L. (1996). Fossil dinoflagellate diversity, originations and extinctions and their significance. Canadian Journal of Botany, 74, 1687–1694.

    Article  Google Scholar 

  • Marshall, A. (1996). Calcification in hermatypic and ahermatypic corals. Science, 271, 1788–1792.

    Article  Google Scholar 

  • Matsuzaki, M., Kuroiwa, H., Kuroiwa, T., Kita, K., & Nozaki, H. (2008). A cryptic algal group unveiled: A plastid biosynthesis pathway in the oyster parasite Perkinsus marinus. Molecular Biology and Evolution, 25, 1167–1179.

    Google Scholar 

  • McMinn, A., & Scot, F. J. (2005). Dinoflagellates, Chapter 3. In F. J. Scott & H. W. Marchant (Eds.), Antarctic marine protists (pp. 202–250). Canberra: Australian Biological Resources Study, Australian Antarctic Division.

    Google Scholar 

  • Mensinger, A. F., & Case, J. F. (1992). Dinoflagellate luminescence increases susceptibility of zooplankton to teleost predation. Marine Biology, 112, 207–210.

    Article  Google Scholar 

  • Meyers, T. R., Koeneman, T. M., Botelho, C., & Short, S. (1987). Bitter crab disease: A fatal dinoflagellate infection and marketing problem for Alaskan Tanner crabs Chionoecetes bairdi. Diseases of Aquatic Organisms, 3, 195–216.

    Article  Google Scholar 

  • Minge, M. A., Shalchian-Tabrizi, K., Tørresen, O. K., Takishita, K., Probert, I., Inagaki, Y., Klaveness, D., & Jakobsen, K. S. (2010). A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMC Evolutionary Biology, 10, 191.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moestrup, Ø., Hansen, G., & Daugbjerg, N. (2008). Studies on woloszynskioid dinoflagellates. III: On the ultrastructure and phylogeny of Borghiella dodgei gen. et sp. nov., a cold-water species from Lake Tovel, N. Italy, and on B. tenuissima comb. nov. (syn. Woloszynskia tenuissima). Phycologia, 47, 54–78.

    Article  CAS  Google Scholar 

  • Moldowan, J. M., & Talyzina, N. M. (1998). Biogeochemical evidence for dinoflagellate ancestors in the early Cambrian. Science, 281, 1168–1170.

    Article  CAS  PubMed  Google Scholar 

  • Moon, E., Nam, S. W., Shin, W., Park, M. G., & Coats, D. W. (2015). Do all dinoflagellates have an extranuclear spindle? Protist, 166, 569–584.

    Article  PubMed  Google Scholar 

  • Moore, R. B., Oborník, M., Januškovec, J., Chrudimský, T., Vancová, M., Green, D. H., Wright, S. W., Davies, N. W., Bolch, C. J. S., Heimann, K., Šlapeta, J., Hoegh-Guldberg, O., Logsdon Jr., J. M., & Carter, D. A. (2008). A photosynthetic alveolate closely related to apicomplexan parasites. Nature, 451, 959–963.

    Article  CAS  PubMed  Google Scholar 

  • Moreira, D., & López-García, P. (2002). The molecular ecology of microbial eukaryotes unveils a hidden world. Trends in Microbiology, 10, 31–38.

    Article  CAS  PubMed  Google Scholar 

  • Morrill, L. C., & Loeblich III, A. R. (1983). Ultrastructure of the dinoflagellate amphiesma. International Review of Cytology, 82, 151–181.

    Article  CAS  PubMed  Google Scholar 

  • Morse, D., Salois, P., Markovic, P., & Hastings, J. W. (1995). A nuclear-encoded form II rubisco in dinoflagellates. Science, 268, 1622–1624.

    Article  CAS  PubMed  Google Scholar 

  • Netzel, H., & Dürr, G. (1984). Dinoflagellate cell cortex, Chapter 3. In D. L. Spector (Ed.), Dinoflagellates. New York: Academic.

    Google Scholar 

  • Nicolas, M. T., Johnson, C. H., Bassot, J. M., & Hastings, J. W. (1985). Immunogold labeling of organelles in the bioluminescent dinoflagellate Gonyaulax polyedra with anti- luciferase antibody. Cell Biology International Reports, 9, 797–802.

    Article  CAS  PubMed  Google Scholar 

  • Nisbet, R. E. R., Koumadou, V. L., Barbrook, A. C., & Howe, C. J. (2004). Novel plastid gene minicircles in the dinoflagellate Amphidinium operculatum. Gene, 331, 141–147.

    Article  PubMed  CAS  Google Scholar 

  • Nishitani, G., Nagai, S., Hayakawa, S., Kosaka, Y., Sakurada, K., Kamiyama, T., & Gojobori, T. (2012). Multiple plastids collected by the dinoflagellate Dinophysis mitra through kleptoplastidy. Applied and Environmental Microbiology, 78, 813–821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nosenko, T., Lidie, K. L., Van Dolah, F. M., Lindquist, E., & Cheng, J. F. (2006). U.S. Department of Energy-Joint Genome Institute, Bhattacharya, D.: Chimeric plastid proteome in the Florida red tide dinoflagellate Karenia brevis. Molecular Biology and Evolution, 23, 2026–2038.

    Article  CAS  PubMed  Google Scholar 

  • Oakley, B., & Dodge, J. D. (1974). Kinetochores associated with the nuclear envelope in the mitosis of a dinoflagellate. Journal of Cell Biology, 63, 322–325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto, N., Horák, A., & Keeling, P. (2012). Description of two species of early-branching dinoflagellates, Psammosa pacifica n. g., n. sp., and Psammosa atlantica n. sp. PLOS One, 7. doi:10.1371/journal.pone.0034900.

    Google Scholar 

  • Onuma, R., & Horiguchi, T. (2015). Kleptochloroplast enlargement, karyoklepty and the distribution of the cryptomonad nucleus in Nusuttodinium aeruginosum (Dinophyceae). Protist, 166, 177–195.

    Article  CAS  PubMed  Google Scholar 

  • Orr, R. J. S., Murray, S. A., Stüken, A., Rhodes, L., & Jakobsen, K. S. (2012). When naked became armored: An eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLOS One. doi:10.1371/journal.pone.0050004.

    Google Scholar 

  • Patron, N. J., Waller, R. F., & Keeling, P. J. (2006). A tertiary plastid uses genes from two endosymbionts. Journal of Molecular Biology, 357, 1373–1382.

    Article  CAS  PubMed  Google Scholar 

  • Pfiester, L. A., & Anderson, D. M. (1987). Dinoflagellate life-cycles and their environmental control, Chapter 14. In F. J. R. Taylor (Ed.), The biology of dinoflagellates. Oxford: Blackwell.

    Google Scholar 

  • Pollingher, U. (1987). Freshwater ecosystems, Chapter 11. In F. J. R. Taylor (Ed.), The biology of dinoflagellates. Oxford: Blackwell.

    Google Scholar 

  • Poupin, J., Cussatlegras, A.-S., & Geistdoerfer, P. (1999). Plancton marin bioluminescent. Brest: Rapport scientifique du Laboratoire d’Océanographie de l’École Navale LOEN, 83 pp.

    Google Scholar 

  • Pross, J., Kotthof, U., & Zonnefeld, K. (2004). Organic-walled dinoflagellate cysts as paleoenvironmental indicators in the Meso- and Cenozoic. Palaeontologische Zeitschrift, 78, 5–39.

    Article  Google Scholar 

  • Rae, P. M. M. (1976). Hydroxymethiluracil in eukaryote DNA: A natural feature of the Pyrrophyta (dinoflagellates). Science, 194, 1062–1064.

    Article  CAS  PubMed  Google Scholar 

  • Raikov, I. B. (1994). The diversity of forms of mitosis in protozoa: A comparative review. European Journal of Protistology, 30, 253–269.

    Article  Google Scholar 

  • Ris, H., & Kubai, D. F. (1974). An unusual mitotic mechanism in the parasitic protozoan Syndinium sp. Journal of Cell Biology, 60, 702–720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizzo, P. J. (1991). The enigma of the dinoflagellate chromosome. Journal of Protozoology, 38, 246–252.

    Article  Google Scholar 

  • Sako, Y., Yoshida, T., Uchida, A., Arakawa, O., Noguchi, T., & Ishida, Y. (2001). Purification and characterization of a sulfotransferase specific to N-21 of saxitoxin and gonyautoxin 2 + 3 from the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). Journal of Phycology, 37, 1044–1051.

    Article  CAS  Google Scholar 

  • Saldarriaga, J. F., Taylor, F. J. R., Cavalier-Smith, T., Menden-Deuer, S., & Keeling, P. J. (2004). Molecular data and the evolutionary history of dinoflagellates. European Journal of Protistology, 40, 85–111.

    Article  Google Scholar 

  • Sánchez-Puerta, M. V., Lippmeier, J. C., Apt, K. E., & Delwiche, C. F. (2007). Plastid genes in a non-photosynthetic dinoflagellate. Protist, 158, 105–117.

    Article  PubMed  CAS  Google Scholar 

  • Sarjeant, W. A. S. (1974). Fossil and living dinoflagellates. London: Academic.

    Google Scholar 

  • Schiller, J. (1933, 1937). In Rabenhorst’s Kryptogamen Flora, 10(3) Teil. 1,2.

    Google Scholar 

  • Schnepf, E., & Elbrächter, M. (1992). Nutritional strategies in dinoflagellates: A review with emphasis on cell biological aspects. European Journal of Protistology, 28, 3–24.

    CAS  PubMed  Google Scholar 

  • Schnepf, E., & Elbrächter, M. (1999). Dinophyte chloroplasts and phylogeny-a review. Grana, 38, 81–97.

    Article  Google Scholar 

  • Schweikert, M., & Elbrächter, M. (2004). First ultrastructural investigations of the consortium between a phototrophic eukaryotic endosymbiont and Podolampas bipes (Dinophyceae). Phycologia, 43, 614–623.

    Article  Google Scholar 

  • Sellers, C.G., Gast, R. J. & Sanders, R. W. (2014). Selective feeding and foreign plastid retention in an Antarctic dinoflagellate. Journal of Phycology, 50, 1081–1088.

    Article  CAS  PubMed  Google Scholar 

  • Silberman, J. D., Collins, A. G., Gershwin, L. A., Johnson, P. J., & Roger, A. J. (2004). Ellobiopsids of the genus Thalassomyces are alveolates. Journal of Eukaryotic Microbiology, 51, 246–252.

    Article  PubMed  Google Scholar 

  • Skovgaard, A., Meneses, I., & Angélico, M. M. (2009). Identifying the lethal fish egg parasite Ichthyodinium chabelardi as a member of Marine Alveolate Group I. Environmental Microbiology, 11, 2030–2041.

    Article  CAS  PubMed  Google Scholar 

  • Slamovits, C. H., & Keeling, P. J. (2008). Plastid-derived genes in the non-photosynthetic alveolate Oxyrrhis marina. Molecular Biology and Evolution, 25, 1297–1306.

    Article  CAS  PubMed  Google Scholar 

  • Smayda, T. J. (1997). What is a bloom? A commentary. Limnology and Oceanography, 42, 1132–1136.

    Article  Google Scholar 

  • Smayda, T. J., & Reynolds, C. S. (2003). Strategies of marine dinoflagellate survival and some rules of assembly. Journal of Sea Research, 49, 95–106.

    Article  Google Scholar 

  • Sournia, A. (1973). Catalogue des espèces et taxons infraspécifiques de Dinoflagellés marins actuels. Beihefte zur Nova Hedwigia, 48, 1–92.

    Google Scholar 

  • Sparmann, S. F., Leander, B. S., & Hoppenrath, M. (2008). Comparative morphology and molecular phylogeny of Apicoporus n. gen.: A new genus of marine benthic dinoflagellates formerly classified within Amphidinium. Protist, 159, 383–399.

    Article  PubMed  Google Scholar 

  • Spector, D. L. (Ed.). (1984). Dinoflagellates. New York: Academic.

    Google Scholar 

  • Spector, D. L., Vasconcelos, A. C., & Triemer, R. E. (1981). DNA duplication and chromosome structure in the dinoflagellates. Protoplasma, 105, 185–194.

    Article  CAS  PubMed  Google Scholar 

  • Steidinger, K. A., & Williams, J. (1970). Memoirs of the Hourglass cruises (Vol. II). St. Petersburg: Marine Research Laboratory.

    Google Scholar 

  • Stelter, K., El-Sayed, N. M., & Seeber, F. (2007). The expression of a plant-type ferredoxin redox system provides molecular evidence for a plastid in the early dinoflagellate Perkinsus marinus. Protist, 158, 119–130.

    Article  CAS  PubMed  Google Scholar 

  • Stentiford, G. D., & Shields, J. D. (2005). A review of the parasitic dinoflagellates Hematodinium species and Hematodinium-like infections in marine crustaceans. Diseases of Aquatic Organisms, 66, 47–70.

    Article  PubMed  Google Scholar 

  • Sweeney, B. M. (1987). Bioluminescence and circadian rhythms. In F. J. R. Taylor (Ed.), The biology of dinoflagellates (Botanical monographs). Oxford: Blackwell.

    Google Scholar 

  • Takano, Y., Hansen, G., Fujita, D., & Horiguchi, T. (2008). Serial replacement of diatom endosymbionts in two freshwater dinoflagellates, Peridiniopsis spp. (Peridiniales, Dinophyceae). Phycologia, 47, 41–53.

    Article  CAS  Google Scholar 

  • Takishita, K., Tsuchiya, M., Kawato, M., Ogun, K., Kitazato, H. & Maruyama, T. (2007). Genetic diversity of microbial eukaryotes in anoxic sediment of the saline meromictic lake Namako-ike (Japan): on the detection of anaerobic or anoxic-tolerant lineages of eukaryotes. Protist, 158, 51–64.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, F. J. R. (1976). Dinoflagellates from the International Indian Ocean Expedition. Biblioteca Botanica, 132, 1–234. pls. 1–46.

    Google Scholar 

  • Taylor, F. J. R. (1980). On dinoflagellate evolution. Biosystems, 13, 65–108.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, F. J. R. (1987). The biology of dinoflagellates (Botanical monographs). Oxford: Blackwell.

    Google Scholar 

  • Taylor, F. J. R. (2004). Illumination or confusion? Dinoflagellate molecular phylogenetic data viewed from a primarily morphological standpoint. Phycological Research, 52, 308–324.

    Article  CAS  Google Scholar 

  • Taylor, F. J. R., Hoppenrath, M., & Saldarriaga, J. F. (2008). Dinoflagellate diversity and distribution. Biodiversity and Conservation, 17, 407–418. Themed issue: Protist diversity and geographical distribution.

    Article  Google Scholar 

  • Terao, K., Ito, E., Kakinuma, Y., Igarashi, K., Kobayashi, M., Ohizumi, Y., & Yasumoto, T. (1989). Histopathological studies on experimental marine toxin poisoning. IV: Pathogenesis of experimental maitotoxin poisoning. Toxicon, 27, 979–988.

    Article  CAS  PubMed  Google Scholar 

  • Trench, R. K. (1997). Diversity of symbiotic dinoflagellates and the evolution of microalgal-invertebrate symbioses. In H. A. Lessios & I. G. MacIntyre (Eds.), Proceedings of the eighth international coral reef symposium 2 (pp. 1275–1286). Balboa: Smithsonian Tropical Research Institute.

    Google Scholar 

  • Triemer, R. E. (1982). A unique mitotic variation in the marine dinoflagellate Oxyrrhis marina (Pyrrophyta). Journal of Phycology, 18, 399–411.

    Article  Google Scholar 

  • Van Dolah, F. M. (2000). Marine algal toxins: Origins, health effects and their increased occurrence. Environmental Health Perspectives, 108(Suppl 1), 133–141.

    Article  PubMed  PubMed Central  Google Scholar 

  • Velo-Suárez, L., Brosnahan, M. L., Anderson, D. M., & McGillicuddy Jr., D. J. (2013). A quantitative assessment of the role of the parasite Amoebophrya in the termination of Alexandrium fundyense blooms within a small coastal embayment. PLoS One. doi:10.1371/journal.pone.0081150.

    PubMed  PubMed Central  Google Scholar 

  • von Stosch, H. A. (1964). Zum Problem der sexuellen Fortplanzung in der Peridineengattung Ceratium. Helgoländer Wissenschaftliche Meeresuntersuchungen, 10, 140–153.

    Article  Google Scholar 

  • Waller, R. F., & Jackson, C. J. (2009). Dinoflagellate mitochondrial genomes: Stretching the rules of molecular biology. BioEssays, 31, 237–245.

    Article  CAS  PubMed  Google Scholar 

  • Watanabe, M. M., Sasa, T., Suda, S., Inouye, I., & Takishi, S. (1991). Major carotenoid composition of an endosymbiont in a green dinoflagellate, Lepidodinium viride. Journal of Phycology, 27(Suppl), 75.

    Google Scholar 

  • Westfall, J. A., Bradbury, P. C., & Townsend, J. W. (1983). Ultrastructure of the dinoflagellate Polykrikos. Journal of Cell Science, 63, 245–261.

    CAS  PubMed  Google Scholar 

  • Whitney, S. M., Shaw, D. C., & Yellowlees, D. (1995). Evidence that some dinoflagellates contain a ribulose-1,5-biphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proceedings of the Royal Society of London Series B, 259, 271–275.

    Article  CAS  PubMed  Google Scholar 

  • Wisecaver, J. H., & Hackett, J. D. (2010). Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genomics, 11, 366.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wong, J. T. Y., New, D. C., Wong, J. C. W., & Hung, V. K. L. (2003). Histone-like proteins of the dinoflagellate Crypthecodinium cohnii have homologies to bacterial DNA-binding proteins. Eukaryotic Cell, 2, 646–650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., & Lin, S. (2005). Mitochondrial cytochrome b mRNA editing in dinoflagellates: Possible ecological and evolutionary associations? Journal of Eukaryotic Microbiology, 52, 538–545.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z., Green, B. R., & Cavalier-Smith, T. (1999). Single gene circles in dinoflagellate plastid genomes. Nature, 400, 155–159.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Bhattacharya, D., & Lin, S. (2005). Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. Journal of Phycology, 41, 411–420.

    Article  CAS  Google Scholar 

  • Zhang, H., Hou, Y., Miranda, L., Campbell, D. A., Sturm, N. R., Gaasterland, T., & Lin, S. (2007). Spliced leader RNA trans-splicing in dinoflagellates. Proceedings of the National Academy of Sciences of the United States of America, 104, 4618–4623.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Saldarriaga, J.F., ‘Max’ Taylor, F.J.R. (2017). Dinoflagellata. In: Archibald, J., Simpson, A., Slamovits, C. (eds) Handbook of the Protists. Springer, Cham. https://doi.org/10.1007/978-3-319-28149-0_22

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