Dinophysis

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Dinophysis
Dinophysis acuminata.jpg
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Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Myzozoa
Superclass: Dinoflagellata
Class: Dinophyceae
Order: Dinophysiales
Family: Dinophysaceae
Genus: Dinophysis
Ehrenberg

Dinophysis is a genus of dinoflagellates [1] [2] [3] common in tropical, temperate, coastal and oceanic waters. [4] It was first described in 1839 by Christian Gottfried Ehrenberg. [5]

Contents

Dinophysis are typically medium-sized cells (30-120 μm). [5] The structural plan and plate tabulation are conserved within the genus. [4] Dinophysis thecae are divided into halves by a sagittal fission suture. [4] There are five types of thecae ornamentation in this genus, [4] and those are a useful character for species identification. [4] Dinophysis mainly divide by binary fission. [4]

Dinophysis chloroplasts are usually rod-shaped or granular and yellow or brown colored. [4] Some Dinophysis spp. take up kleptoplastids when feeding. Toxic Dinophysis produce okadaic acid, dinophysistoxins, and pectenotoxins, which inhibit protein phosphatase and cause diarrhea. [6]

Background

The etymology of this genus name comes from Greek, Dino comes from "deinos" (δεινός) [7] meaning terrible [8] and "physis" (φύσις) meaning nature. [9]

The genus was first described in 1839 by Ehrenberg, which is why the holotype species of this genus is Dinophysis acuta Ehrenberg. [5] It has been found that what were considered different Dinophysis species might just be different life stages. [5]

Severe diarrheic shellfish poisoning breakouts in northeast Japan led to the identification of a Dinophysis species that produces toxins, Dinophysis fortii in 1976–77. [6] This genus is difficult to maintain in culture leading to challenges in gaining knowledge of these organisms. [6] Some Dinophysis spp. have kleptoplastids of cryptomonad origin, specifically from the cryptomonad Teleaulax amphioxeia . [10] Dinophysis caudata have acquired these kleptoplastids by engulfing the ciliate Mesodinium rubrum which has engulfed T. amphioxeia plastids. [10] Cryptomonad plastids have four membranes and a nucleomorph and are a product of secondary endosymbiosis. [10]

For years it was believed that Dinophysis did not have a sexual cycle. [6] However, it is now apparent that gamete cells can form in Dinophysis acuminata and D. acuta; this was found when small, spherical cells seemed to form inside larger ones. [6]

Habitat and ecology

The common habitat of Dinophysis is in tropical, temperate, coastal and oceanic waters. [4] Although most Dinophysis are marine and planktonic, some have been found in coastal lagoons [5]

Dinophysis caudata feed on ciliates, specifically Mesodinium rubrum through myzocytosis. [6] Picophytoplankton, bacteria, and cryptomonads are also likely part of the diet of Dinophysis. [6] For culture, Dinophysis are maintained on mixotrophic nutrition. [6] Although they are mixotrophic, they are mainly phagotrophic and photosynthesis is linked to kleptoplastids. [6]

Description of the organism

Morphology

The typical cell size of Dinophysis ranges from 30 to 120 μm, they are medium-sized cells. [5] It is possible for the cell size of Dinophysis to vary from large, vegetative cells to small, gamete-like cells. [6] Dinophysis have hypothecae that consist of two large plates, which take up most of the space of the theca, as well as some small platelets. [6] The genus is characterized by having 18 plates: four epithecal plates, two small apical plates, four sulcal plates, four cingular plates, and four hypothecal plates. [5] They have a cingulum, which is anteriorly positioned, and the cells are laterally compressed. [6] The structural plan and plate tabulation are conserved within the genus. [4] Dinophysis thecae are divided in halves by a sagittal fission suture. [4] Thecal ornamentation is a useful character for species identification. [4] There are five types of thecae ornamentation in this genus. [4] Type A is a smooth theca or a theca with shallow depressions, a single row of pores lines the anterior and posterior cingular lists and the margins of the large epithecal and hypothecal plates. [4] Type B has a more pitted thecal surface but has fewer pores; Type C is characterized by shallow hexagonal reticulation in the theca and a pore in the middle of each areola. [4] Type D exhibits large, spherical areolation in the thecal surface with pores in the center of every 3-5 areolae; type E is characteristic of laterally flattened Dinophysis and consists of a circular areolation thecal surface and a central pore in nearly all areolae. [4]

Plastids and kleptoplastids

Minute, usually rod-shaped or granular and yellow or brown colored chloroplasts are characteristic of Dinophysis. [4] The chloroplasts have stacks of three thylakoids and an internal pyrenoid. [4] In senescent cells, chloroplasts tend to aggregate in the middle and form orange patches. [4]

Some Dinophysis spp. likely possess plastids from cryptomonad origin, since the plastids are identical to those of the cryptophyte Teleaulax amphioxeia . [11] In this case, the process consisted in the engulfment (incomplete phagocytosis) of the ciliate M. rubrum which in turn engulfed a whole cryptomonad and now only the plastids remain. [11]

There has been debate surrounding whether the plastids of D. caudata are permanent or kleptoplastids. [12] It is now known that the plastids of D. caudata are kleptoplastids and the explanation for the discrepancy among molecular and ultrastructural data is due to structural modification during the acquisition of plastids through feeding. [12] When D. caudata was fed M. rubrum reddish-brown plastids, these were not digested in a food vacuole, rather they were transported to the periphery of the cell to join the rest of the plastids. [12] The plastids that were ingested are surrounded by membrane vesicles and transferred to the cytoplasm. [12] During plastid sequestration, the plastids see a change in morphology, the thylakoids of M. rubrum plastids become irregular and distended. [12] The change in pigment of the plastids is due to photoactivity, the change of low light to high light causes the plastids to turn green when there is no prey. [12] The cryptophyte nucleomorph found in M. rubrum is lost in D. caudata. [12] The final plastids of D. caudata appeared stellate and had clustered pyrenoids terminally positioned, their thylakoid membranes are placed in pairs. [12]

Life cycle

Dinophysis mainly divides asexually by binary fission. [4] For years it was believed that Dinophysis did not have a sexual cycle. [6] However, it is now apparent that gamete cells can form in D. acuminata and D. acuta; this was found when small, spherical cells seemed to form inside larger ones. [6] While the role of a sexual cycle in Dinophysis is not fully understood yet, there is a proposed model for how this works. In the proposed model, vegetative cells give rise to small motile cells (the smaller cells previously observed within the larger cells). The smaller cells then also become vegetative and act like gametes and after conjugation the cells divide and encyst. [13] The smaller cells that give rise to gametes tend to have thinner thecae and less developed cingular and sulcal lists. [13] They also are flagellated and swim, they use their flagella and lists to wrap around another gamete cell for conjugation. [13]

Although the gametes are part of a dimorphic sexual cycle, sex cysts do not play an active role in the seeding of Dinophysis populations. [6]

Pseudogenes

While toxic species of Dinophysis such as D. acuminata have a single gene for LSU rRNA, non-toxic species seem to have two distinct classes of LSU rRNA. [14] The difference between these two classes was a 70 bp deletion, indicating the shorter product might be a pseudogene. [14] The pseudogene can be used as a marker of D. acuminata and might conveniently serve as a marker of toxic and non-toxic strains [14] and bring more insight to the genetics of toxicity of Dinophysis.

Phylogenetics

Dinoflagellates are algae and according to recent phylogeny they are sister groups to ciliates and apicomplexans. [14] Most phylogenetic studies are done with sequences of both large and small ribosomal subunits and do not always agree with morphological studies based on thecal plates. [14] Sequencing of the small subunit of the ribosome of Dinophysis revealed very similar sequences in three species of Dinophysis (D. acuminata, D. norvegica and D. acuta), suggesting that photosynthetic Dinophysis have evolved recently. [14]

Practical importance

Dinophysis are a threat to shellfish aquaculture due to toxic lipophilic shellfish toxins that they produce. [6] Dinophysis have cryptophyte-like pigments and at least seven species of Dinophysis contain diarrheic shellfish toxins. [6]

Toxic Dinophysis produce okadaic acid, dinophysistoxins, and pectenotoxins, which inhibit protein phosphatase and produce diarrhea. [6] The more dominant the okadates are, the higher the impact on public health. [6] Toxins are secondary metabolites, and, in some cases, a single species can produce multiple types of toxins. [6] The production of these is controlled by both genetic factors and the environment. [6] The enzymes produced vary due to the environment in which Dinophysis grow. [6] The boreal seas, temperate seas and tropical seas are where most assemblages of Dinophysis that cause diarrheic shellfish poisoning occur. [6] Common features associated with toxic Dinophysis include: large sizes, highly developed cingular and sulcal lists and hypothecal processes. [6]

Species

Related Research Articles

<span class="mw-page-title-main">Dinoflagellate</span> Unicellular algae with two flagella

The dinoflagellates are a monophyletic group of single-celled eukaryotes constituting the phylum Dinoflagellata and are usually considered protists. Dinoflagellates are mostly marine plankton, but they also are common in freshwater habitats. Their populations vary with sea surface temperature, salinity, and depth. Many dinoflagellates are photosynthetic, but a large fraction of these are in fact mixotrophic, combining photosynthesis with ingestion of prey.

Cryptomonas is the name-giving genus of the Cryptomonads established by German biologist Christian Gottfried Ehrenberg in 1831. The algae are common in freshwater habitats and brackish water worldwide and often form blooms in greater depths of lakes. The cells are usually brownish or greenish in color and are characteristic of having a slit-like furrow at the anterior. They are not known to produce any toxins. They are used to feed small zooplankton, which is the food source for small fish in fish farms. Many species of Cryptomonas can only be identified by DNA sequencing. Cryptomonas can be found in several marine ecosystems in Australia and South Korea.

<span class="mw-page-title-main">Kleptoplasty</span> Form of algae symbiosis

Kleptoplasty or kleptoplastidy is a process in symbiotic relationships whereby plastids, notably chloroplasts from algae, are sequestered by the host. The word is derived from Kleptes (κλέπτης) which is Greek for thief. The alga is eaten normally and partially digested, leaving the plastid intact. The plastids are maintained within the host, temporarily continuing photosynthesis and benefiting the host.

<i>Gymnodinium</i> Genus of single-celled organisms

Gymnodinium is a genus of dinoflagellates, a type of marine and freshwater plankton. It is one of the few naked dinoflagellates, or species lacking armor known as cellulosic plates. Since 2000, the species which had been considered to be part of Gymnodinium have been divided into several genera, based on the nature of the apical groove and partial LSU rDNA sequence data. Amphidinium was redefined later. Gymnodinium belong to red dinoflagellates that, in concentration, can cause red tides. The red tides produced by some Gymnodinium, such as Gymnodinium catenatum, are toxic and pose risks to marine and human life, including paralytic shellfish poisoning.

<span class="mw-page-title-main">Cryptophyceae</span> Class of single-celled organisms

The cryptophyceae are a class of algae, most of which have plastids. About 230 species are known, and they are common in freshwater, and also occur in marine and brackish habitats. Each cell is around 10–50 μm in size and flattened in shape, with an anterior groove or pocket. At the edge of the pocket there are typically two slightly unequal flagella.

<i>Karenia</i> (dinoflagellate) Genus of single-celled organisms

Karenia is a genus that consists of unicellular, photosynthetic, planktonic organisms found in marine environments. The genus currently consists of 12 described species. They are best known for their dense toxic algal blooms and red tides that cause considerable ecological and economical damage; some Karenia species cause severe animal mortality. One species, Karenia brevis, is known to cause respiratory distress and neurotoxic shellfish poisoning (NSP) in humans.

<i>Peridinium</i> Genus of single-celled organisms

Peridinium is a genus of motile, marine and freshwater dinoflagellates. Their morphology is considered typical of the armoured dinoflagellates, and their form is commonly used in diagrams of a dinoflagellate's structure. Peridinium can range from 30 to 70 μm in diameter, and has very thick thecal plates.

<span class="mw-page-title-main">Dinophyceae</span> Class of single-celled organisms

Dinophyceae is a class of dinoflagellates.

<i>Rhodomonas</i> Genus of single-celled organisms

Rhodomonas is a genus of cryptomonads. It is characterized by its red colour, the square-shaped plates of its inner periplast, its short furrow ending in a gullet, and a distinctly shaped chloroplast closely associated with its nucleomorph. Historically, Rhodomonas was characterized by its red chloroplast alone, but this no longer occurs as its taxonomy has become increasingly based on molecular and cellular data. Currently, there is some debate about the taxonomic validity of Rhodomonas as a genus and further research is needed to verify its taxonomic status. Rhodomonas is typically found in marine environments, although freshwater reports exist. It is commonly used as a live feed for various aquaculture species.

<i>Ornithocercus</i> Genus of single-celled organisms

Ornithocercus is a genus of planktonic dinoflagellate that is known for its complex morphology that features considerable lists growing from its thecal plates, giving an attractive appearance. Discovered in 1883, this genus has a small number of species currently categorized but is widespread in tropical and sub-tropical oceans. The genus is marked by exosymbiotic bacteria gardens under its lists, the inter-organismal dynamics of which are a current field of research. As they reside only in warm water, the genus has been used as a proxy for climate change and has potential to be an indicator species for environmental change if found in novel environments.

Mesodinium chamaeleon is a ciliate of the genus Mesodinium. It is known for being able to consume and maintain algae endosymbiotically for days before digesting the algae. It has the ability to eat red and green algae, and afterwards using the chlorophyll granules from the algae to generate energy, turning itself from being a heterotroph into an autotroph. The species was discovered in January 2012 outside the coast of Nivå, Denmark by professor Øjvind Moestrup.

<i>Alexandrium</i> (dinoflagellate) Genus of single-celled organisms

Alexandrium is a genus of dinoflagellates. It contains some of the dinoflagellate species most harmful to humans, because it produces toxic harmful algal blooms (HAB) that cause paralytic shellfish poisoning (PSP) in humans. There are about 30 species of Alexandrium that form a clade, defined primarily on morphological characters in their thecal plates.

<i>Dinophysis acuminata</i> Species of dinoflagellate

Dinophysis acuminata is a marine plankton species of dinoflagellates that is found in coastal waters of the north Atlantic and Pacific oceans. The genus Dinophysis includes both phototrophic and heterotrophic species. D. acuminata is one of several phototrophic species of Dinophysis classed as toxic, as they produce okadaic acid which can cause diarrhetic shellfish poisoning (DSP). Okadiac acid is taken up by shellfish and has been found in the soft tissue of mussels and the liver of flounder species. When contaminated animals are consumed, they cause severe diarrhoea. D. acuminata blooms are constant threat to and indication of diarrhoeatic shellfish poisoning outbreaks.

<i>Mesodinium rubrum</i> Species of single-celled organism

Mesodinium rubrum is a species of ciliates. It constitutes a plankton community and is found throughout the year, most abundantly in spring and fall, in coastal areas. Although discovered in 1908, its scientific importance came into light in the late 1960s when it attracted scientists by the recurrent red colouration it caused by forming massive blooms, that cause red tides in the oceans.

<i>Dinophysis acuta</i> Species of dinoflagellate

Dinophysis acuta is a species of flagellated planktons belonging to the genus Dinophysis. It is one of the few unusual photosynthetic protists that acquire plastids from algae by endosymbiosis. By forming massive blooms, particularly in late summer and spring, it causes red tides. It produces toxic substances and the red tides cause widespread infection of seafood, particularly crabs and mussels. When infected animals are consumed, severe diarrhoea occurs. The clinical symptom is called diarrhetic shellfish poisoning. The main chemical toxins were identified in 2006 as okadaic acid and pectenotoxins. They can produce non-fatal or fatal amounts of toxins in their predators, which can become toxic to humans.

<i>Tripos</i> (dinoflagellate) Genus of single-celled organisms

Tripos is a genus of marine dinoflagellates in the family Ceratiaceae. It was formerly part of Ceratium, then separated out as Neoceratium, a name subsequently determined to be invalid.

Durinskia is a genus of dinoflagellates that can be found in freshwater and marine environments. This genus was created to accommodate its type species, Durinskia baltica, after major classification discrepancies were found. While Durinskia species appear to be typical dinoflagellates that are armored with cellulose plates called theca, the presence of a pennate diatom-derived tertiary endosymbiont is their most defining characteristic. This genus is significant to the study of endosymbiotic events and organelle integration since structures and organelle genomes in the tertiary plastids are not reduced. Like some dinoflagellates, species in Durinskia may cause blooms.

<i>Mesodinium</i> Genus of single-celled organisms

Mesodinium is a genus of ciliates that are widely distributed and are abundant in marine and brackish waters.

Coolia is a marine dinoflagellate genus in the family Ostreopsidaceae. It was first described by Meunier in 1919. There are currently seven identified species distributed globally in tropical and temperate coastal waters. Coolia is a benthic or epiphytic type dinoflagellate: it can be found adhered to sediment or other organisms but it is not limited to these substrates. It can also be found in a freely motile form in the water column. The life cycle of Coolia involves an asexual stage where the cell divides by binary fission and a sexual stage where cysts are produced. Some of the species, for example, Coolia tropicalis and Coolia malayensis, produce toxins that can potentially cause shellfish poisoning in humans.

<i>Octactis</i> Genus of unicellular protists

Octactis is a genus of silicoflagellates, marine photosynthetic unicellular protists that take the form of either flagellates or axopodial amoebae. Described by Josef Schiller in 1925, Octactis contains various species of marine phytoplankton, some of them responsible for algal blooms that are toxic to fish.

References

  1. AlgaeBase: Dinophysis Ehrenberg, 1839
  2. NCBI: Dinophysis Ehrenberg, 1839 (genus); graphically: Dinophysis, Lifemap NCBI Version.
  3. WoRMS: Dinophysis Ehrenberg, 1839
  4. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Hallegraeff, G.M., Lucas, I.A.N. 1988: The marine dinoflagellate genus Dinophysis (Dinophyceae): photosynthetic, neritic and non-photosynthetic, oceanic species. Phycologia, 27: 25–42. 10.2216/i0031-8884-27-1-25.1
  5. 1 2 3 4 5 6 7 Ehrenberg, C.G., 1839. Über jetzt wirklich noch zahlreich lebende Thier-Arten der Kreideformatien der Erde. Königlich Preussische Akademie der Wissenschaften zu Berlin, Bericht über die zur Bekanntmachung geeigneten Verhandlungen, 1839, p. 152-159. Über noch zahlreich jetzt lebende Thierarten der Kreidebildung, nach Vorträgen in der Akademie der Wissenschaften zu Berlin in den Jahren 1839 und 1840, L. Voss, Leipzig. PDF, p. 44ff
  6. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Reguera, B. et al. 2012. Harmful Dinophysis species: A review. Harmful Algae, 14: 87–106. 10.1016/j.hal.2011.10.016
  7. ΔεινόςΔεινός - Wiktionary, en.wiktionary.org/wiki/δεινός.
  8. Anon, dino | Search Online Etymology Dictionary. Index. Available at: https://www.etymonline.com/search?q=dino [Accessed February 12, 2018].
  9. Physis” Wikipedia, Wikimedia Foundation, 20 Apr. 2018, en:Physis.[ circular reference ]
  10. 1 2 3 Kim, J. I., Yoon, H. S., Yi, G., Kim, H. S., Yih, W., & Shin, W. 2015: The plastid genome of the cryptomonad teleaulax amphioxeia. PLoS One, 10(6). doi : 10.1371/journal.pone.0129284
  11. 1 2 Janson, S. & Granéli, E. 2003: Genetic Analysis of The psbA gene from Single Cells Indicates a Cryptomonad Origin of the Plastid in Dinophysis (Dinophyceae).” Phycologia, 42(5): 473–477. doi:10.2216/i0031-8884-42-5-473.1.
  12. 1 2 3 4 5 6 7 8 Kim, M., Nam, S. W., Shin, W., Coats, D. W. and Park, M. G. 2012: Dinophysis caudata (Dinophyceae) sequesters and retains plastids from the mixotrophic ciliate prey Mesodinium Rubrum. Journal of Phycology, 48: 569-579. doi:10.1111/j.1529-8817.2012.01150.x
  13. 1 2 3 Berland, Br, et al., 1995. Observations on possible life cycle stages of the dinoflagellates Dinophysis cf. acuminata, Dinophysis acuta and Dinophysis pavillardi. Aquatic Microbial Ecology, 9: 183–189.
  14. 1 2 3 4 5 6 Rehnstam-Holm, A.-S., Godhe, A. & Anderson, D.M., 2002. Molecular studies of Dinophysis (Dinophyceae) species from Sweden and North America. Phycologia, 41: 348–357.10.2216/i0031-8884-41-4-348.1

Further reading