Accessible Requires Authentication Published by De Gruyter July 19, 2013

Cell division in Azadinium spinosum (Dinophyceae)

Urban Tillmann and Malte Elbrächter
From the journal Botanica Marina


Azadinium spinosum is a planktonic dinoflagellate, and a source of azaspiracids, a group of lipophilic toxins of human health concern. Little is known about the biology of this genus, and its phylogenetic position within the Dinophyceae is not yet fully resolved. Here, we present detailed observations regarding its vegetative cell division. As a first sign of cell division, the round interphase nucleus enlarges and becomes elongate in a slightly oblique orientation. The nucleus then divides along its longitudinal axis. Cytokinesis of A. spinosum occurs in motile cells and is of the desmoschisis type, i.e., the parental theca is shared between the two sister cells. Divided cells completely separate before the thecal plates are fully replaced. The anterosinistral daughter cell keeps the parent cell’s apex, including the apical pore complex and all the apical and epithecal intercalary plates, whereas the posterodextral daughter cell keeps, among others, both antapical plates. In general, the course of the fission line follows the plate overlap pattern and is, with a few exceptions, similar to other species of the Gonyaulacales. A literature survey shows that both desmoschisis and eleuteroschisis have been described for Gonyaulacales and Peridiniales, which suggests that mode of division may not be a good ordinal criterion for classification.

Corresponding author: Urban Tillmann, Alfred Wegener Institute, Am Handelshafen12, 27570 Bremerhaven, Germany

Thanks to Fridel Hinz for help with the electron microscope and Consuelo Carbonell-Moore for comments and help with the English. The comments of Matthew Dring and two anonymous reviewers improved the paper and are greatly acknowledged.


Bhaud, Y., D. Guillebault, J.F. Lennon, H. Defacque, M.O. Soyer-Gobillard and H. Moreau. 2000. Morphology and behaviour of dinoflagellate chromosomes during the cell cycle and mitosis. J. Cell. Sci. 113: 1231–1239. Search in Google Scholar

Braarud, T. 1945. Morphological observations on marine dinoflagellate cultures. Avhandlinger Utgitt Av Det Norske Videnskaps-Academi Oslo. I. Mat.-Naturv. Klasse 1944 11: 1–18. Search in Google Scholar

Buchanan, R.J. 1968. Studies at Oyster Bay in Jamaica, West Indies. IV. Observations on the morphology and asexual cycle of Pyrodinium bahamense Plate. J. Phycol. 4: 272–277. Search in Google Scholar

Carbonell-Moore, M.C. 1994. On the taxonomy of the family Podolampadaceae Lindemann (Dinophyceae) with descriptions of three new genera. Rev. Palaeobot. Palyno. 84: 73–99. Search in Google Scholar

Diwald, K. 1938. Die ungeschlechtliche und geschlechtliche Fortpflanzung von Glenodinium lubiniensiforme spec. nov. Flora oder Allgemeine Botanische Zeitung 132: 174–192. Search in Google Scholar

Dodge, J.D. 1963. The nucleus and nuclear division in the Dinophyceae. Arch. Protistenkd. 106: 442–452. Search in Google Scholar

Dodge, J.D. 1988. An SEM study of the thecal division in Gonyaulax (Dinophyceae). Phycologia 27: 241–247. Search in Google Scholar

Dürr, G. and H. Netzel. 1974. The fine structure of the cell surface in Gonyaulax polyedra (Dinoflagellatea). Cell Tiss. Res. 150: 21–41. Search in Google Scholar

Elbrächter, M. 1973. Population dynamics of Ceratium in coastal waters of the Kiel Bay. Oikos 15: 43–48. Search in Google Scholar

Elbrächter, M. 2003. Dinophyte reproduction: progress and conflicts. J. Phycol. 39: 629–632. Search in Google Scholar

Entz, G. 1904. Beiträge zur Kenntnis der Peridineen. Mathematische und naturwissenschaftliche Berichte aus Ungarn 20: 96–144. Search in Google Scholar

Fensome, R.A., F.J.R. Taylor, G. Norris, W.A.S. Sarjeant, D.I. Wharton and G.L. Williams. 1993. A classification of living and fossil dinoflagellates. Micropaleontology, Special Publication 7: 1–351. Search in Google Scholar

Figueroa, R.I. and I. Bravo. 2005. Sexual reproduction and two different encystment strategies of Lingulodinium polyedrum (Dinophyceae) in culture. J. Phycol. 41: 370–379. Search in Google Scholar

Figueroa, R.I., E. Garcés and I. Bravo. 2007. Comparative study on the life cycles of Alexandrium tamutum and Alexandrium minutum (Gonyaulacales, Dinophyceae) in culture. J. Phycol. 43: 1039–1053. Search in Google Scholar

Figueroa, R.I., I. Bravo and E. Garcés. 2008. The significance of sexual versus asexual cyst formation in the life cycle of the noxious dinoflagellate Alexandrium peruvianum. Harmful Algae 7: 653–663. Search in Google Scholar

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. Search in Google Scholar

Garces, E., M. Delgado, M. Maso and J. Camp. 1998. Life history and in situ growth rates of Alexandrium taylori. J. Phycol. 34: 880–887. Search in Google Scholar

Gomez, F., D. Moreira and P. Lopez-Garcia. 2010. Molecular phylogeny of the dinoflagellates Podolampas and Blepharocysta (Peridiniales, Dinophyceae). Phycologia 49: 212–220. Search in Google Scholar

Gottschling, M., S. Soehner, C. Zinssmeiste, U. John, J. Plötner, M. Schweikert, K. Aligizaki and M. Elbrächter. 2012. Delimitation of the Thoracosphaeraceae (Dinophyceae), including the calcareous dinoflagellates, based on large amounts of ribosomal RNA sequence data. Protist 163: 15–24. Search in Google Scholar

Happach-Kasan, C. 1982. Beobachtungen zum Bau der Theka von Ceratium cornutum (Ehrenb.) Clap. et Lachm. (Dinophyta). Arch. Protistenkd. 128: 181–207. Search in Google Scholar

Hickel, B. and U. Pollingher. 1986. On the morphology and ecology of Gonyaulax apiculata (Penard) Entz from the Selenter See (West Germany). Arch. Hydrobiol. Suppl. 73: 227–232. Search in Google Scholar

Kita, T., Y. Fukuyo, H. Tokuda and R. Hirano. 1993. Sexual reproduction of Alexandrium hiranoi (Dinophyceae). Bull. Plankton Soc. Jpn. 39: 79–85. Search in Google Scholar

Kofoid, C.A. 1911. Dinoflagellates of the San Diego region IV. The genus Gonyaulax, with notes on its skeletal morphology and a discussion of its generic and specific characters. Univ. Calif. Publ. Zool. 8: 187–286. Search in Google Scholar

Krock, B., U. Tillmann, D. Voß, B.P. Koch, R. Salas, M. Witt, E. Potvin and H.J. Jeong. 2012. New azaspiracids in Amphidomataceae (Dinophyceae): proposed structures. Toxicon 60: 830–839. Search in Google Scholar

Leadbeater, B.S.C. and J.D. Dodge. 1967. An electron microscope study of nuclear and cell division in a dinoflagellate. Arch. Mikrobiol. 57: 239–254. Search in Google Scholar

Lewis, J., A. Rochon and M. Ellegaard. 2001. The cyst-theca relationship of Bitectatodinium tepikiense (Dinophyceae). J. Phycol. 36: 137–146. Search in Google Scholar

Loeblich, A.R., III. 1970. The amphiesma or dinoflagellate cell covering. Proc. North Am. Paleontol. Conv. 1969 Part G.: 867–929. Search in Google Scholar

McMahon, T. and J. Silke. 1996. West coast of Ireland; winter toxicity of unknown aetiology in mussels. Harmful Algae News 14: 2. Search in Google Scholar

Montresor, M. 1995. The life history of Alexandrium pseudogonyaulax (Gonyaulacales, Dinophyceae). Phycologia 34: 444–448. Search in Google Scholar

Montresor, M. and D. Marino. 1994. New observations on the life cycle of Pyrophacus horologium Stein (Dinophyceae). Bolletino della Società Adriatica di Scienze 75: 261–268. Search in Google Scholar

Morrill, L.C. and A.R. Loeblich, III. 1981. A survey for body scales in dinoflagellates and a revision of Cachonina and Heterocapsa (Pyrrhophyta). J. Plankton Res. 3: 53–65. Search in Google Scholar

Morrill, L.C. and A.R. Loeblich, III. 1984. Cell division and reformation of the amphiesma in the pelliculate dinoflagellate, Heterocapsa niei. J. Mar. Biol. Ass. UK 64: 939–953. Search in Google Scholar

Netzel, H. 1982. Cytological and ecological aspects of morphogenesis and structure of recent and fossil protist-skeletons: dinoflagellates. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 164: 64–74. Search in Google Scholar

Netzel, H. and G. Dürr. 1984. Dinoflagellate Cell Cortex. In: (D.L. Spector, ed.) Dinoflagellates. Academic Press Inc., Orlando. pp. 43–105. Search in Google Scholar

Netzel, H., H. Gocht, G. Dürr and W. Holwein. 1978. Cytological and ecological aspects of morphogenesis and structure of recent and fossil protistan skeletons. a) Dinoflagellates. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 157: 69–77. Search in Google Scholar

Nézan, E., U. Tillmann, G. Bilien, S. Boulben, K. Chèze, F. Zentz, R. Salas and N. Chomérat. 2012. Taxonomic revision of the dinoflagellate Amphidoma caudata: transfer to the genus Azadinium (Dinophyceae) and proposal of two varieties, based on morphological and molecular phylogenetic analyses. J. Phycol. 48: 925–939. Search in Google Scholar

Pfiester, L.A. and D.M. Anderson. 1987. Dinoflagellate reproduction. In: (F.J.R. Taylor, ed.) The biology of dinoflagellates. Academic Press, New York. pp. 611–648. Search in Google Scholar

Pholpunthin, P., Y. Fukuyo, K. Matsuoka and Y. Nimura. 1999. Life history of a marine dinoflagellate Pyrophacus steinii (Schiller) Wall et Dale. Bot. Mar. 42: 189–197. Search in Google Scholar

Salas, R., U. Tillmann, U. John, J. Kilcoyne, A. Burson, C. Cantwell, P. Hess, T. Jauffrais and J. Silke. 2011. The role of Azadinium spinosum (Dinophyceae) in the production of azasdpiracid shellfish poisoning in mussels. Harmful Algae 10: 774–783. Search in Google Scholar

Saldarriaga, J.F., F.J.R. Taylor, T. Cavalier-Smith, S. Menden-Deuer and P.J. Keeling. 2004. Molecular data and the evolutionary history of dinoflagellates. Eur. J. Protistol. 40: 85–111. Search in Google Scholar

Schweikert, M. and M. Elbrächter. 2004. First ultrastructural investigations of the consortium between phototrophic eukaryotic endocytobiont and Podolampas bipes (Dinophyceae). Phycologia 43: 614–623. Search in Google Scholar

Skovgaard, A. 1996. Engulfment of Ceratium spp. (Dinophyceae) by the thecate photosynthetic dinoflagellate Fragilidium subglobosum. Phycologia 35: 490–499. Search in Google Scholar

Spector, D.L. 1984. Dinoflagellate nuclei. In: (D.L. Spector, ed.) Dinoflagellates. Academic Press Inc., Orlando. pp. 107–147. Search in Google Scholar

Steidinger, K.A. and J. Williams. 1970. Dinoflagellates. Memoirs of the Hourglass Cruises 2: 1–251. Search in Google Scholar

Taylor, F.J.R. 2004. Illumination or confusion? Dinoflagellate molecular phylogenetic data viewed from a primarily morphological standpoint. Phycol. Res. 52: 308–324. Search in Google Scholar

Tillmann, U. and M. Elbrächter. 2010. Plate overlap pattern of Azadinium spinosum Elbrächter et Tillmann (Dinophyceae), the newly discovered primary source of azaspiracid toxins. In: (K.C. Ho, M.J. Zhou, Y.Z. Qi, eds.) Proceedings of the 13th International Conference on Harmful Algae. Environmental Publication House, Hong Kong. pp. 42–44. Search in Google Scholar

Tillmann, U. and M. Hoppenrath. 2013. Life cycle of the pseudocolonial dinoflagellate Polykrikos kofoidii (Gymnodiniales, Dinoflagellata). J. Phycol. 49: 298–317. Search in Google Scholar

Tillmann, U., M. Elbrächter, B. Krock, U. John and A. Cembella. 2009. Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. Eur. J. Phycol. 44: 63–79. Search in Google Scholar

Tillmann, U., M. Elbrächter, U. John, B. Krock and A. Cembella. 2010. Azadinium obesum (Dinophyceae), a new nontoxic species in the genus that can produce azaspiracid toxins. Phycologia 49: 169–182. Search in Google Scholar

Tillmann, U., M. Elbrächter, U. John and B. Krock. 2011. A new non-toxic species in the dinoflagellate genus Azadinium: A. poporum sp. nov. Eur. J. Phycol. 46: 74–87. Search in Google Scholar

Tillmann, U., S. Soehner, E. Nézan and B. Krock. 2012a. First record of Azadinium from the Shetland Islands including the description of A. polongum sp. nov. Harmful Algae 20: 142–155. Search in Google Scholar

Tillmann, U., R. Salas, M. Gottschling, B. Krock, D. O’Drisol and M. Elbrächter. 2012b. Amphidoma languida sp. nov. (Dinophyceae) reveals a close relationship between Amphidoma and Azadinium. Protist 163: 701–719. Search in Google Scholar

Tomas, R.N. 1974. Cell division in Gonyaulax catenella, a marine catenate dinoflagellate. J. Protozool. 21: 316–321. Search in Google Scholar

von Stosch, H.A. 1969. Dinoflagellaten aus der Nordsee II. Helgolandinium subglobosum gen et spec. nov. Helgol. wiss. Meeresunters. 19: 569–577. Search in Google Scholar

Walker, L.M. and K. Steidinger. 1979. Sexual reproduction in the toxic dinoflagelate Gonyaulax monilata. J. Phycol. 15: 312–315. Search in Google Scholar

Zhang, H., D. Bhattacharya and S. Lin. 2007. A three-gene dinoflagellate phylogeny suggests monophyly of prorocentrales and a basal position for Amphidinium and Heterocapsa. J. Mol. Evol. 65: 463–474. Search in Google Scholar

Received: 2013-3-6
Accepted: 2013-6-12
Published Online: 2013-07-19
Published in Print: 2013-08-01

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