DESCRIPTION OF THE PHYLUM DINOFLAGELLATA

EUKARYA> CHROMALVEOLATA> ALVEOLATAE> DINOFLAGELLATA

Dinoflagellata (di-no-fla-ghe-LA-ta) is made of two roots, one Greek and one Latin that mean eddy, as in spinning water (din-e -δίνη); and whip (flagellum). The reference is to motile or flagellated cells that spin as they swim.

INTRODUCTION TO THE DINOFLAGELLATA

The dinoflagellates produce distinctive motile cells that are divided into an anterior ( epitheca ) and a posterior ( hypotheca ), separated by a groove called the cingulum (Figure 1). The motile cells have two flagella inserted in the center of the ventral portion of the cell. It is encircled by a ribbon-like flagellum that lies in the cingulum, and the recurrent flagellum , which is whiplash , lies in a groove on the hypotheca called a sulcus (Figure 2). Many taxa are photosynthetic with characteristic chlorophylls (Chlorophylls A and C) and accessory pigments like peridinin. Photosynthetic dinoflagellates are among the most important primary producers in the oceans, and they can dominate in some freshwater and brackish water environments.

The alveolate cell covering in dinoflagellates has been modified in many taxa to form an armored theca (also called an amphiesma) that is made of overlapping cellulosic plates (Figures 3-5). Among the armored taxa, the plate tabulation is very conserved and useful in specific identifications. The particular number of plates can vary enormously from group to group. Prorocentrum has reduced the theca to two major plates (Figure 8).

Dinoflagellates are the main taxa that occur as zooxanthellae, photosynthetic symbionts in many animals, particularly the corals for which they provide food and the ability to sequester calcium carbonate (Figure 6), but when the animals are under stress (thermal, carbon dioxide, ammonium, etc.) they expel the zooxanthellae thus forming “bleached” coral. Many dinoflagellates live in symbiotic relationships that range from mutualism (as in the corals) to parasitism. For example, Syndinium is parasitic within marine microcrustaceans (Figure 7) whose cells it invades. Then, the feeding cell enlarges and undergoes mitosis without cytokinesis to form a plasmodium. Finally, gymnodinoid cells, which may be infective, emerge from the lysed host cell.

Some of the dinoflagellates are predaceous and feed on algae (Figure 9) and other organisms. Pfiesteria is an organism that recently was discovered and has an elaborate lifecycle. It can produce neurotoxins and powerful tissue-dissolving enzymes that enable a population of these cells to kill and consume large fish like striped bass. Stylodinium (Figure 9) and its relatives live as amoeboid cells that feed on filamentous algae after which they form a distinctive structure from which small gymnodinoid cells emerge.

Noctiluca (Figure 10) is a large bioluminescent species that feeds on smaller protists in the marine plankton (I). Its cell is large, vacuolated, and it has a single feeding tentacle. When disturbed at night, Noctiluca, which literally means “night light” produces a soft green light. I have witnessed concentrations of them in the Atlantic and Gulf of Mexico such that the sea and beach glowed an eerie green. Other more typical dinoflagellates like Pyrodinium, also are bioluminescent. They occur in great concentrations in mangrove lagoons in places like Puerto Rico where they play an important role in ecotourism on the island. Many dinoflagellates exhibit bioluminescence such that an older name of the phylum was Pyrrhophyta, the fire plants.

Some dinoflagellates are important as toxin producers and are principle contributors to paralytic shellfish poisoning (PSP), a condition that can occur when filter-feeding bivalves concentrate toxic algae, usually contributors to red tides, and sequester their poisons. Ptychodiscus (=Karenia) brevis is the organism responsible for red tides off the coast of Florida by the production of saxitoxin, a powerful neurotoxin that is second in its lethality only to botulism toxin (Figure 2). Other red tide species occur along most coasts.

Most dinoflagellate species have a characteristic nucleus called a dinokaryon that has bottlebrush condensed chromosomes and no histones. The seemingly primitive nature of the chromosomes and nucleus made them appear to be remnants of the earliest eukaryotes. However, molecular and ultrastructural work confirm that the dinokaryon is a derived character.

The typical life cycle of dinoflagellates is haplontic, that is, the dominant phase of the life history is haploid (Figure 11). For most, the zygote is the only haploid cell and meiosis occurs within the zygocyst. Noctiluca, however, has a diplontic life cycle and meiosis occurs as the first step in gametogenesis.


FIGURE 1. An SEM micrograph of Gymnodinium. Note the ribbon-flagellum in the cingulum. Image from Systematic Biodiversity Image Archive	FIGURE 2. An SEM micrograph of Karenia, the causative agent of red tide around Florida. Note the cells show the dorsal and ventral sides of the cells to illustrate the ribbon-like flagellum in the cingulum and a recurrent whiplash flagellum. Image from http://www.marcobueno.net/arquivos_estudo/arquivo_estudo.asp?txtIDArquivo=343	FIGURE 3. A light micrograph of Ceratium, a large armored plankter of marine and freshwater environments. Image from http://www.vims.edu/~jeff/dinos.htm	FIGURE 4. An SEM micrograph of a Peridinium zygote. Note the armored plates with intercalary bands between them. Image from Systematics Biodiversity Image Archive	FIGURE 5. An SEM micrograph of Dinophysis, a distinctive armored taxon with an apical cingulum and winged extensions of its hypothecal plates. Image from http://www.biol.tsukuba.ac.jp/~inouye/ino/d/Dinophysis1.GIF

FIGURE 6. Symbiodinium is a dinoflagellate that enters into symbiotic relationships with corals and other cnidarians. The coral with its symbionts (left) usually is brightly colored. When the animals are under stress, they begin to expel the symbionts (right). Image from NOAA and in the Public Domain.	FIGURE 7. Parasitic Syndinium cells taken from an infected copepod. Image from http://www.vims.edu/~jeff/dinos.htm	FIGURE 8. An SEM micrograph of Prorocentrum, which has two major plates and the flagellar insertions are at the apex (to the left of this cell). Image from http://www.utas.edu.au/docs/plant_science/Aquatic/pplay/pplaysem03.jpg	FIGURE 9. SEM micrographs of Stylodinium feeding on a green algal filament. Image from a collection of photographs given to me by Lois Pfiester.	FIGURE 10. Noctiluca, a large vacuolated cell that has a feeding tentacle (see it emerge from the cell at right center) is a common member of the marine plankton and is bioluminescent (text with tooltip) . Image from http://www.marcobueno.net/arquivos_estudo/arquivo_estudo.asp?txtIDArquivo=343

FIGURE 11. Typical life cycles of dinoflagellates. Most dinoflagellates have haplontic life cycles. That is, the only diploid cell in the life history is the zygote which undergoes meiosis. Of those, many hologamous, the vegetative cell is also a functional gamete. A few go through a developmental stage in which gametes are formed from vegetative cells. Noctiluca (the lower life history) is diplontic in which the vegetative cell is diploid. During its gametogenesis, the products of meiosis divide many times and develop into isogametes, which are the only dinoflagellate-type cells in the life history. Image from Taylor (1987).

The dinoflagellates have been classified as algae, protists, and protozoa during the past 30 years [Taylor (1987; 1990), Lee (1980), Loeblich (1976), Dodge (1973), Sze (1986), Margulis and Schwartz (1988 and 1998), and Sleigh et al. (1984)] and usually have been divided into two groups. The taxonomy of Bold and Wynne (1985) was more complex with 4 classes, including the enigmatic Ebriids and a separate class for the prorocentrids. A newer taxonomic scheme by Taylor (1990) had only a single class with much more splitting among orders (up to 17). Traditionally, protozoological manuals such as Lee et al. (1985), Kudo (1966) and Grell (1973) lumped the dinoflagellates with all other flagellated unicells (and often with the amoeboid taxa)!

The dinoflagellates appeared to be unrelated to the other chlorophyll c-containing organisms (Dodge, 1989), and differences in nuclear chromosome structure led Dodge (1973) to suggest that the dinoflagellates occupied their own kingdom. However, Taylor (1976) suggested a connection between the dinoflagellates and ciliates, an association which was supported by the 5S rRNA sequence analyses of Hori and Osawa (1987, cited in Dodge 1989). More recent evidence (Gajadhar et al. 1991; Cavalier-Smith 1993; Patterson 1999; Taylor 1999; and Baldauf 2003a) supported the association of the Dinoflagellata, Apicomplexata, and Ciliophora in a larger taxonomic entity called the Alveolata.

The system that we follow has 3 classes of typical dinoflagellates with 11 orders (in a subphylum we call Dinophytina). It was modified from Dodge and Lee (2000), which, itself, was a modification of Fensome et al. (1993). Major taxonomic treatments like Dodge and Lee (2000) have been based primarily on morphology and life history with little or no molecular confirmation.

Molecular phylogenetic studies of the dinoflagellates have been informative relative to the deep-branching taxa only. For example, Saunders et al. (1997) suggested that Noctiluca was a sister to the other dinoflagellates, but and some taxa, like Gymnodinium, were decidedly polyphyletic based on SSU rDNA. Saldarriaga et al. (2003), Hoppenrath and Leander (2010), Gomez et al. (2010), and Fukuda and Endoh (2008) through the use of multiple protein and nucleic acid phylogenies, show that Oxyrrhis (Figure 12) and Perkinsus (Figure 13) are sisters to the rest of the dinoflagellates. Indeed, Perkensus is a parasite of bivalve mollusks and seems to be transitional between dinoflagellates and apicomplexans. The general relationships of taxa in Figure 14 seem to be well-supported. This does seem to indicate not only are the dinoflagellates sisters to the Apicomplexata, a phylum of obligate parasites, but also the basal taxa of dinoflagellates are parasitic.

The signal from nucleic acid sequences and amino acid sequences have not been sufficient to resolve the taxonomy of the dinoflagellates, particularly to the ordinal level (Gomez et al. 2009 and 2010; Murray et al. 2005; Zhang et al. 2005; Leander and Keeling 2004). Perhaps, the difficulties with molecular comparisons is a consequence of extreme genomic modifications in the nuclear (Zhang et al. 2009) and the mitochondrial genomes (Waller et al. 2009).


FIGURE 12. Oxyrrhis, a motile cell that resembles Syndinium motile cells but lacks a semblance of a cingulum. Image from http://microscope.mbl.edu/scripts/	FIGURE 13. Perkensus, a parasite of bivalve mollusks that seems to bridge the dinoflagellates and apicomplexans. Image from http://microscope.mbl.edu/scripts/

FIGURE 14. A cladogram showing the relationships between the higher taxa of the Dinoflagellata (taxa in the shaded box) according to our interpretation of Gomez et al. (2010) within the Alveolatae (taxa in bold, clade A). Within the Dinoflagellata, Perkinsiphytine and Oxyrrhiniphytina are basal groups. The taxa of the Dinophytina (DI) are in a nested series of higher taxa with the symbiotic/parasitic taxa at the base.

LITERATURE CITED

Baldauf, S. L. 2003a. The deep roots of eukaryotes. Science. 300 (5626): 1701-1703.

Bold, H. C. and M. J. Wynne. 1985. Introduction to the Algae. 2nd Edition. Prentice-Hall, Inc. Englewood Cliffs. NJ.

Bütschli, O. 1883–1887. Protozoa. Abtheilung II. Mastigophora. In: Bronn, H. G., ed. Klassen und Ordungen des Thier-Reichs. C. F. Winter, Leipzig. 1: 617–1097.

Cavalier-Smith, T. 1993. Kingdom protozoa and its 18 Phyla. Microbiological Reviews. 57: 953-994.

Dodge, J. D. 1973. The fine structure of algal cells. Academic Press. New York.

Dodge, J. D. 1989. Phylogeny of dinoflagellates and their plastids. In: Green, J.C., B.S.C. Leadbeater, and W.L. Diver, eds. The chromophyte algae: problems and perspectives. Systematics Association Special Volume No. 38. Clarendon Press. Oxford. pp. 207-227.

Dodge, J. D. and J. J. Lee. 2000. Phylum Dinoflagellata. In Lee, J.J., Leedale, G. F. & Bradbury, P., eds. An Illustrated Guide to the Protozoa, Second Edition, vol. 1. Society of Protozoologists, Lawrence, Kansas. pp. 656-689.

Gajadhar, A. A., W. C. Marquardt, R. Hall, J. Gunderson, E. V. A. Carmona, and M. L. Sogin. 1991. Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata, and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. Molecular and Biochemical Parasitology. 45:147-154.

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

Fukuda, Y. and H. Endoh. 2008. Phylogenetic analyses of the dinoflagellate Noctiluca scintillans based on β-tubulin and Hsp90 genes. European Journal of Protistology. 44: 27-33.

Gomez, F., D. Moreira, and P. Lopez-Garcia. 2009. Life cycle and molecular phylogeny of the dinoflagellates Chytriodinium and Dissodinium, ectoparasites of copepod eggs. European Journal of Protistology. 45: 260-270.

Gomez, F., D. Moreira, and P. Lopez-Garcia. 2010. Molecular phylogeny of noctilucoid dinoflagellates (Noctilucales, Dinophyceae). Protist. 161: 466-478.

Grell, K. G. 1973. Protozoology. Springer-Verlag. New York.

Harper, J. T., E. Waanders, and P. J. Keeling. 2005. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. International Journal of Systematic and Evolutionary Microbiology. 55: 487-496.

Hoppenrath, M. and B. S. Leander. 2010. Dinoflagellate phylogeny as inferred from heat shock protein 90 and ribosomal gene sequences. PLoS ONE. 5(10):e13220. doi:10.1371/journal.pone.0013220
Hoppenrath, M., T. R. Bachvaroff, S. M. Handy, C. F. Delwiche, and B. S. Leander. 2009. Molecular phylogeny of ocelloid-bearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences. BMC Evolutionary Biology. 9: 116 doi:10.11186/1471-2148-9-116

Hori, H. and S. Osawa. 1987. Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Molecular Biology and Evolution. 4:445-472.

Keeling P. J. 2004 The diversity and evolutionary history of plastids and their hosts. American Journal of Botany. 91(10): 1481-1493.

Kudo, R. R. 1966. Protozoology. 5th ed. Charles C. Thomas Publisher. Springfield.

Leander, B. S. and P. J. Keeling. 2004. Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from Hsp90 and actin phylogenies. Journal of Phycology. 40: 341-350.

Lee, R. E. 1980. Phycology. Cambridge University Press. Cambridge.

Lee, R. E. 1995. Phycology. 2nd Edition. Cambridge University Press. Cambridge.

Lee, J. J., S. H. Hunter, and E. C. Bovee, eds. 1985. An Illustrated Guide to the Protozoa. Society of Protozoologists. Lawrence, Kansas.

Loeblich, A.R. 1976. Dinoflagellate evolution: speculation and evidence. Journal of Protozoology. 23: 13-28.

Margulis, L. and K. Schwartz. 1988. Five kingdoms, an illustrated guide to the phyla of life on earth. 2nd Edition. W.H. Freeman and Co. New York.

Margulis, L. and K. Schwartz. 1998. Five kingdoms, an illustrated guide to the phyla of life on earth. 3rd Edition. W. H. Freeman and Company. New York.

Murray, S., M. F. Jorgensen, S. Y. W. Ho, D. J. Patterson, and L. S. Jermiin. 2005. Improving the analysis of dinoflagellate phylogeny based on rDNA. Protist. 156: 269-286.

Patterson, D. J. 1999. The diversity of eukaryotes. American Naturalist. 154 (Suppl.): S96–S124.

Saldarriaga, J. F., M. L. McEwan, N. M. Fast, F. J. R. Talyor. and P. J. Keeling. 2003. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology. 53:355-365.

Saunders, G. W., D. R. A. Hill, J. P. Sexton, and R. A. Andersen. 1997. Small-subunit ribosomal RNA sequences from selected dinoflagellates: testing classical evolutionary hypotheses with molecular systematic methods. In: Bhattacharya, D. Origins of Algae and their Plastids (Plant Systematics and Evolution Supplement). Springer Verlag. Vienna. pp. 237-259.

Sleigh, M.A., J.D. Dodge and D.J. Patterson. 1984. Kingdom Protista. In: Barnes, R.K.S., ed. A Synoptic Classification of Living Organisms. Sinauer Associates, Inc. Sunderland, Mass.

Sze, P. 1986. A Biology of the Algae. Wm. C. Brown Publishers. Dubuque, Iowa.

Taylor, F. J. R. 1976. Flagellate Phylogeny: A Study in Conflicts. Journal of Protozoology. 23: 28-40.

Taylor, F. J. R. 1987. Taxonomy and Classification. In: Taylor, F.J.R., ed. The Biology of Dinoflagellates. Botanical Monographs vol. 21. Blackwell Scientific Publications. Oxford.

Taylor, F. J. R. 1990. Dinoflagellata. In: Margulis, L., J.O. Corliss, M. Melkonian, and D.J. Chapman, eds. 1990. Handbook of the Protoctista; the structure, cultivation, habits and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett Publishers. Boston. pp. 419-437.

Taylor, F. J. R. 1999. Ultrastructure as a control for protistan molecular phylogeny. The American Naturalist. 154(supplement): S125-S136.

Waller, R. F. and C. J. Jackson. 2009. Dinoflagellate mitochondrial genomes: stretching the rules of molecular biology. BioEssays. 31: 237-245.

Zhang, H., D. A. Campbell, N. R. Sturm, and S. Lin. 2009. Dinoflagellate splices leader RNA genes display a variety of sequences and genomic arrangements. Molecular Biology and Evolution. 26(8): 1757-1771.

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

By Jack R. Holt. Last revised: 03/03/2013

Diversity of Life

DESCRIPTION OF THE PHYLUM DINOFLAGELLATA

DESCRIPTION OF THE PHYLUM DINOFLAGELLATA (BÜTSCHLI 1885)

DESCRIPTION OF THE PHYLUM DINOFLAGELLATA (BÜTSCHLI 1885)

Document Footer