In terms of number of species, dinoflagellates are one of the largest groups of marine eukaryotes, although substantially smaller thandiatoms.[8] Some species areendosymbionts of marine animals and play an important part in the biology ofcoral reefs. Other dinoflagellates are unpigmented predators on other protozoa, and a few forms areparasitic (for example,Oodinium andPfiesteria). Some dinoflagellates produce resting stages, called dinoflagellate cysts ordinocysts, as part of their lifecycles; this occurs in 84 of the 350 described freshwater species and a little more than 10% of the known marine species.[9][10] Dinoflagellates arealveolates possessing twoflagella, the ancestral condition ofbikonts.
About 1,555 species of free-living marine dinoflagellates are currently described.[11] Another estimate suggests about 2,000 living species, of which more than 1,700 are marine (free-living, as well as benthic) and about 220 are from fresh water.[12] The latest estimates suggest a total of 2,294 living dinoflagellate species, which includes marine, freshwater, and parasitic dinoflagellates.[2]
A rapid accumulation of certain dinoflagellates can result in a visible coloration of the water, colloquially known asred tide (aharmful algal bloom), which can causeshellfish poisoning if humans eat contaminated shellfish. Some dinoflagellates also exhibitbioluminescence, primarily emitting blue-green light, which may be visible in oceanic areas under certain conditions.
The term "dinoflagellate" is a combination of the Greekdinos and the Latinflagellum.Dinos means "whirling" and signifies the distinctive way in which dinoflagellates were observed to swim.Flagellum means "whip" and this refers to theirflagella.[13]
In 1753, the first modern dinoflagellates were described byHenry Baker as "Animalcules which cause the Sparkling Light in Sea Water",[14] and named byOtto Friedrich Müller in 1773.[15] The term derives from the Greek word δῖνος (dînos), meaning whirling, and Latinflagellum, a diminutive term for a whip or scourge.
In the 1830s, the German microscopistChristian Gottfried Ehrenberg examined many water and plankton samples and proposed several dinoflagellate genera that are still used today includingPeridinium, Prorocentrum, andDinophysis.[16]
These same dinoflagellates were first defined byOtto Bütschli in 1885 as theflagellate order Dinoflagellida.[17] Botanists treated them as a division of algae, namedPyrrophyta orPyrrhophyta ("fire algae"; Greekpyrr(h)os, fire) after the bioluminescent forms, orDinophyta. At various times, thecryptomonads,ebriids, andellobiopsids have been included here, but only the last are now considered close relatives. Dinoflagellates have a known ability to transform from noncyst to cyst-forming strategies, which makes recreating their evolutionary history extremely difficult.
Dinoflagellates are unicellular and possess two dissimilar flagella arising from the ventral cell side (dinokont flagellation). They have a ribbon-like transverse flagellum with multiple waves that beats to the cell's left, and a more conventional one, the longitudinal flagellum, that beats posteriorly.[18][19][20] The transverse flagellum is a wavy ribbon in which only the outer edge undulates from base to tip, due to the action of the axoneme which runs along it. The axonemal edge has simple hairs that can be of varying lengths. The flagellar movement produces forward propulsion and also a turning force. The longitudinal flagellum is relatively conventional in appearance, with few or no hairs. It beats with only one or two periods to its wave. The flagella lie in surface grooves: the transverse one in the cingulum and the longitudinal one in the sulcus, although its distal portion projects freely behind the cell. In dinoflagellate species with desmokont flagellation (e.g.,Prorocentrum), the two flagella are differentiated as in dinokonts, but they are not associated with grooves.
Dinoflagellates have a complex cell covering called anamphiesma or cortex, composed of a series of membranes, flattenedvesicles called alveoli (= amphiesmal vesicles) and related structures.[21][22] In thecate ("armoured") dinoflagellates, these support overlappingcellulose plates to create a sort of armor called thetheca or lorica, as opposed to athecate ("nude") dinoflagellates. These occur in various shapes and arrangements, depending on the species and sometimes on the stage of the dinoflagellate. Conventionally, the term tabulation has been used to refer to this arrangement ofthecal plates. The plate configuration can be denoted with the plate formula or tabulation formula. Fibrousextrusomes are also found in many forms.[23][24]
A transverse groove, the so-called cingulum (or cigulum) runs around the cell, thus dividing it into an anterior (episoma) and posterior (hyposoma). If and only if a theca is present, the parts are called epitheca and hypotheca, respectively. Posteriorly, starting from the transverse groove, there is a longitudinal furrow called the sulcus. The transverse flagellum strikes in the cingulum, the longitudinal flagellum in the sulcus.[25][24]
Together with various other structural and genetic details, this organization indicates a close relationship between the dinoflagellates, theApicomplexa, andciliates, collectively referred to as thealveolates.[23]
Most Dinoflagellates have a plastid derived from secondary endosymbiosis of red algae, however dinoflagellates with plastids derived from green algae and tertiary endosymbiosis of diatoms have also been discovered.[27] Similar to other photosynthetic organisms, dinoflagellates containchlorophyllsa and c2 and the carotenoid beta-carotene. Dinoflagellates also produce thexanthophylls includingperidinin,dinoxanthin, anddiadinoxanthin. Thesepigments give many dinoflagellates their typical golden brown color. However, the dinoflagellatesKarenia brevis,Karenia mikimotoi, andKarlodinium micrum have acquired other pigments through endosymbiosis, includingfucoxanthin.[28] This suggests their chloroplasts were incorporated by severalendosymbiotic events involving already colored or secondarily colorless forms. The discovery ofplastids in theApicomplexa has led some to suggest they were inherited from an ancestor common to the two groups, but none of the more basal lines has them. All the same, the dinoflagellate cell consists of the more common organelles such as rough and smoothendoplasmic reticulum,Golgi apparatus,mitochondria,lipid andstarch grains, and foodvacuoles. Some have even been found with a light-sensitive organelle, theeyespot or stigma, or a larger nucleus containing a prominentnucleolus. The dinoflagellateErythropsidinium has the smallest known eye.[29]
'Core dinoflagellates' (dinokaryotes) have a peculiar form ofnucleus, called adinokaryon, in which thechromosomes are attached to thenuclear membrane. These carry reduced number ofhistones. In place of histones, dinoflagellate nuclei contain a novel, dominant family of nuclear proteins that appear to be of viral origin, thus are calledDinoflagellate viral nucleoproteins (DVNPs) which are highly basic, bind DNA with similar affinity to histones, and occur in multiple posttranslationally modified forms.[31] Dinoflagellate nuclei remain condensed throughout interphase rather than just duringmitosis, which is closed and involves a uniquely extranuclearmitotic spindle.[32] This sort of nucleus was once considered to be an intermediate between the nucleoid region ofprokaryotes and the true nuclei ofeukaryotes, so were termed "mesokaryotic", but now are considered derived rather than primitive traits (i. e. ancestors of dinoflagellates had typical eukaryotic nuclei). In addition to dinokaryotes, DVNPs can be found in a group of basal dinoflagellates (known as MarineAlveolates, "MALVs") that branch as sister to dinokaryotes (Syndiniales).[33]
Theperidinin dinoflagellates, named after their peridinin plastids, appear to be ancestral for the dinoflagellate lineage. Almost half of all known species have chloroplasts, which are either the original peridinin plastids or new plastids acquired from other lineages of unicellular algae through endosymbiosis. The remaining species have lost their photosynthetic abilities and have adapted to a heterotrophic, parasitic orkleptoplastic lifestyle.[34][35]
Most (but not all) dinoflagellates have adinokaryon, described below (see:Life cycle, below). Dinoflagellates with a dinokaryon are classified underDinokaryota, while dinoflagellates without a dinokaryon are classified underSyndiniales.
Although classified aseukaryotes, the dinoflagellate nuclei are not characteristically eukaryotic, as some of them lackhistones andnucleosomes, and maintain continually condensed chromosomes duringmitosis. The dinoflagellate nucleus was termed 'mesokaryotic' by Dodge (1966),[36] due to its possession of intermediate characteristics between the coiled DNA areas of prokaryotic bacteria and the well-defined eukaryotic nucleus. This group, however, does contain typically eukaryoticorganelles, such as Golgi bodies, mitochondria, and chloroplasts.[37]
Dinophytic microalga isolated from sediments ofAmur Bay
Jakob Schiller (1931–1937) provided a description of all the species, both marine and freshwater, known at that time.[38] Later, Alain Sournia (1973, 1978, 1982, 1990, 1993) listed the new taxonomic entries published after Schiller (1931–1937).[39][40][41][42][43] Sournia (1986) gave descriptions and illustrations of the marine genera of dinoflagellates, excluding information at the species level.[44] The latest index is written by Gómez.[2]
English-language taxonomic monographs covering large numbers of species are published for the Gulf of Mexico,[45] the Indian Ocean,[46] the British Isles,[47] the Mediterranean[48] and the North Sea.[49]
The main source for identification of freshwater dinoflagellates is theSüsswasser Flora.[50]
Calcofluor-white can be used to stain thecal plates in armoured dinoflagellates.[51]
Dinoflagellates are found in all aquatic environments: marine, brackish, and fresh water, including in snow or ice. They are also common in benthic environments and sea ice.
AllZooxanthellae are dinoflagellates and most of them are members within Symbiodiniaceae (e.g. the genusSymbiodinium).[52] The association betweenSymbiodinium and reef-buildingcorals is widely known. However, endosymbionticZooxanthellae inhabit a great number of other invertebrates and protists, for example manysea anemones,jellyfish,nudibranchs, the giant clamTridacna, and several species ofradiolarians andforaminiferans.[53] Many extant dinoflagellates areparasites (here defined as organisms that eat their prey from the inside, i.e.endoparasites, or that remain attached to their prey for longer periods of time, i.e. ectoparasites). They can parasitize animal or protist hosts.Protoodinium, Crepidoodinium, Piscinoodinium, andBlastodinium retain their plastids while feeding on their zooplanktonic or fish hosts. In most parasitic dinoflagellates, the infective stage resembles a typical motile dinoflagellate cell.
Three nutritional strategies are seen in dinoflagellates:phototrophy,mixotrophy, andheterotrophy. Phototrophs can bephotoautotrophs orauxotrophs.Mixotrophic dinoflagellates are photosynthetically active, but are also heterotrophic. Facultative mixotrophs, in which autotrophy or heterotrophy is sufficient for nutrition, are classified as amphitrophic. If both forms are required, the organisms are mixotrophicsensu stricto. Some free-living dinoflagellates do not have chloroplasts, but host a phototrophic endosymbiont. A few dinoflagellates may use alien chloroplasts (cleptochloroplasts), obtained from food (kleptoplasty). Some dinoflagellates may feed on other organisms as predators or parasites.[54]
Food inclusions contain bacteria, bluegreen algae, diatoms, ciliates, and other dinoflagellates.[55][56][57][58][59][60][61]
Mechanisms of capture and ingestion in dinoflagellates are quite diverse. Several dinoflagellates, both thecate (e.g.Ceratium hirundinella,[60]Peridinium globulus[58]) and nonthecate (e.g.Oxyrrhis marina,[56]Gymnodinium sp.[62] andKofoidinium spp.[63]), draw prey to the sulcal region of the cell (either via water currents set up by the flagella or via pseudopodial extensions) and ingest the prey through the sulcus. In severalProtoperidinium spp., e.g.P. conicum, a large feeding veil—a pseudopod called the pallium—is extruded to capture prey which is subsequently digestedextracellularly (= pallium-feeding).[64][65]Oblea,Zygabikodinium, andDiplopsalis are the only other dinoflagellate genera known to use this particular feeding mechanism.[65][66][67]Gymnodinium fungiforme, commonly found as a contaminant in algal or ciliate cultures, feeds by attaching to its prey and ingesting prey cytoplasm through an extensible peduncle.[68] Two related genera,Polykrikos andNeatodinium, shoot out a harpoon-like organelle to capture prey.[69]
Some mixotrophic dinoflagellates are able to produce neurotoxins that have anti-grazing effects on larger copepods and enhance the ability of the dinoflagellate to prey upon larger copepods. Toxic strains ofKarlodinium veneficum produce karlotoxin that kills predators who ingest them, thus reducing predatory populations and allowing blooms of both toxic and non-toxic strains ofK. veneficum. Further, the production of karlotoxin enhances the predatory ability ofK. veneficum by immobilizing its larger prey.[70]K. armiger are more inclined to prey upon copepods by releasing a potent neurotoxin that immobilizes its prey upon contact. WhenK. armiger are present in large enough quantities, they are able to cull whole populations of their copepod prey.[71]
The feeding mechanisms of the oceanic dinoflagellates remain unknown, although pseudopodial extensions were observed inPodolampas bipes.[72]
Dinoflagellates possess a distinctive suite of photosynthetic pigments that allow them to survive and grow in a variety of aquatic environments. Like other phytoplankton, many dinoflagellates contain chlorophyll a and chlorophyll c, which are essential for photosynthesis and light energy capture.[73] However, unlike green algae and higher plants, they lack chlorophyll b. Instead, they utilize chlorophyll c2, which is more efficient for absorbing blue-green light, making them well adapted to low-light or deeper water conditions.[74] These pigments, along with carotenoids, contribute to the characteristic coloration of dinoflagellates, which can range from golden-brown to red.
A unique pigment in dinoflagellates is peridinin, a specialized carotenoid that plays a key role in light harvesting and energy transfer to chlorophyll a.[75] Peridinin is highly efficient in capturing blue light, which penetrates deeper into the water column, giving many dinoflagellates a competitive advantage in stratified or turbid environments.[76] Additionally, dinoflagellates contain other carotenoids such as diadinoxanthin and dinoxanthin, which play important roles in photoprotection by dissipating excess light energy and preventing oxidative stress under high irradiance.[77] These pigments are necessary for photoacclimation, allowing dinoflagellates to survive under fluctuating light conditions.
Not all dinoflagellates rely solely on photosynthetic pigments for energy. Many species are heterotrophic or mixotrophic, meaning they can acquire nutrients through both photosynthesis and predation.[78] Symbiotic dinoflagellates, such as Symbiodinium, play a important ecological role by forming mutualistic relationships with corals, where their pigments drive photosynthesis and energy production that sustain coral reef ecosystems.[79] The unique pigment composition of dinoflagellates also contributes to large-scale phenomena such as harmful algal blooms and red tides, where high concentrations of pigmented cells cause dramatic discoloration of coastal waters and can produce toxic effects.[80]
Dinoflagellate blooms are generally unpredictable, short, with low species diversity, and with little species succession.[81] The low species diversity can be due to multiple factors. One way a lack of diversity may occur in a bloom is through a reduction in predation and a decreased competition. The first may be achieved by having predators reject the dinoflagellate, by, for example, decreasing the amount of food it can eat. This additionally helps prevent a future increase in predation pressure by causing predators that reject it to lack the energy to breed. A species can then inhibit the growth of its competitors, thus achieving dominance.[82]
Dinoflagellates sometimes bloom in concentrations of more than a million cells per millilitre. Under such circumstances, they can produce toxins (generally calleddinotoxins) in quantities capable of killing fish and accumulating in filter feeders such asshellfish, which in turn may be passed on to people who eat them. This phenomenon is called ared tide, from the color the bloom imparts to the water. Some colorless dinoflagellates may also form toxic blooms, such asPfiesteria. Some dinoflagellate blooms are not dangerous. Bluish flickers visible in ocean water at night often come from blooms ofbioluminescent dinoflagellates, which emit short flashes of light when disturbed.
Algal bloom (akasio) byNoctiluca spp. in Nagasaki
A red tide occurs because dinoflagellates are able to reproduce rapidly and copiously as a result of the abundant nutrients in the water. Although the resulting red waves are an interesting visual phenomenon, they containtoxins that not only affect all marine life in the ocean, but the people who consume them as well.[83] A specific carrier isshellfish. This can introduce both nonfatal and fatal illnesses. One such poison issaxitoxin, a powerfulparalyticneurotoxin.[84][85][86]
Human inputs ofphosphate further encourage these red tides, so strong interest exists in learning more about dinoflagellates, from both medical and economic perspectives. Dinoflagellates are known to be particularly capable of scavenging dissolved organic phosphorus for P-nutrient, several HAS species have been found to be highly versatile and mechanistically diversified in utilizing different types of DOPs.[84][85][86] The ecology ofharmful algal blooms is extensively studied.[87]
Long exposure image of bioluminescence ofN. scintillans in the yacht port ofZeebrugge, BelgiumKayaking inthe Bioluminescent Bay, Vieques, Puerto Rico
At night, water can have an appearance of sparkling light due to the bioluminescence of dinoflagellates.[88][89] More than 18 genera of dinoflagellates are bioluminescent,[90] and the majority of them emit a blue-green light.[91] These species containscintillons, individual cytoplasmic bodies (about 0.5 μm in diameter) distributed mainly in the cortical region of the cell, outpockets of the main cell vacuole. They containdinoflagellate luciferase, the main enzyme involved in dinoflagellate bioluminescence, andluciferin, a chlorophyll-derived tetrapyrrole ring that acts as the substrate to the light-producing reaction. The luminescence occurs as a brief (0.1 sec) blue flash (max 476 nm) when stimulated, usually by mechanical disturbance. Therefore, when mechanically stimulated—by boat, swimming, or waves, for example—a blue sparkling light can be seen emanating from the sea surface.[92]
Dinoflagellate bioluminescence is controlled by a circadian clock and only occurs at night.[93] Luminescent and nonluminescent strains can occur in the same species. The number of scintillons is higher during night than during day, and breaks down during the end of the night, at the time of maximal bioluminescence.[94]
The luciferin-luciferase reaction responsible for the bioluminescence is pH sensitive.[92] When the pH drops, luciferase changes its shape, allowing luciferin, more specifically tetrapyrrole, to bind.[92] Dinoflagellates can use bioluminescence as a defense mechanism. They can startle their predators by their flashing light or they can ward off potential predators by an indirect effect such as the "burglar alarm". The bioluminescence attracts attention to the dinoflagellate and its attacker, making the predator more vulnerable to predation from higher trophic levels.[92]
Bioluminescent dinoflagellate ecosystem bays are among the rarest and most fragile,[95] with the most famous ones being the Bioluminescent Bay inLa Parguera, Lajas, Puerto Rico; Mosquito Bay inVieques, Puerto Rico; and Las Cabezas de San Juan Reserva NaturalFajardo, Puerto Rico. Also, a bioluminescent lagoon is near Montego Bay, Jamaica, and bioluminescent harbors surround Castine, Maine.[96] Within the United States, Central Florida is home to theIndian River Lagoon which is abundant with dinoflagellates in the summer and bioluminescent ctenophore in the winter.[97]
Dinoflagellates have ahaplontic life cycle, with the possible exception ofNoctiluca and its relatives.[5] The life cycle usually involves asexual reproduction by means of mitosis, either throughdesmoschisis oreleuteroschisis. More complex life cycles occur, more particularly with parasitic dinoflagellates. Sexual reproduction also occurs,[100] though this mode of reproduction is only known in a small percentage of dinoflagellates.[101] This takes place by fusion of two individuals to form azygote, which may remain mobile in typical dinoflagellate fashion and is then called a planozygote. This zygote may later form a resting stage orhypnozygote, which is called adinoflagellate cyst ordinocyst. After (or before) germination of the cyst, the hatchling undergoesmeiosis to produce newhaploid cells. Dinoflagellates appear to be capable of carrying out severalDNA repair processes that can deal with different types ofDNA damage.[102]
Dinoflagellata life cycle: 1-mitosis, 2-sexual reproduction, 3-planozygote, 4-hypnozygote, 5-planomeiocyte
The life cycle of dinoflagellates, including possible described transitions [103]
The life cycle of many dinoflagellates includes at least one nonflagellated benthic stage as acyst. Different types of dinoflagellate cysts are mainly defined based on morphological (number and type of layers in the cell wall) and functional (long- or short-term endurance) differences. These characteristics were initially thought to clearly distinguishpellicle (thin-walled) cysts fromresting (double-walled) dinoflagellate cysts. The former were considered short-term (temporal) and the latter long-term (resting) cysts. However, during the last two decades further knowledge has highlighted the great intricacy of dinoflagellate life histories.[103]
More than 10% of the approximately 2000 known marine dinoflagellate species produce cysts as part of their life cycle (see diagram on the right). These benthic phases play an important role in the ecology of the species, as part of a planktonic-benthic link in which the cysts remain in the sediment layer during conditions unfavorable for vegetative growth and, from there, reinoculate the water column when favorable conditions are restored.[103]
Indeed, during dinoflagellate evolution the need to adapt to fluctuating environments and/or to seasonality is thought to have driven the development of this life cycle stage. Most protists form dormant cysts in order to withstand starvation and UV damage.[104] However, there are enormous differences in the main phenotypic, physiological and resistance properties of each dinoflagellate species cysts. Unlike in higher plants most of this variability, for example indormancy periods, has not been proven yet to be attributed to latitude adaptation or to depend on other life cycle traits.[105][106] Thus, despite recent advances in the understanding of the life histories of many dinoflagellate species, including the role of cyst stages, many gaps remain in knowledge about their origin and functionality.[103]
Recognition of the capacity of dinoflagellates to encyst dates back to the early 20th century, inbiostratigraphic studies of fossil dinoflagellate cysts.Paul Reinsch was the first to identify cysts as the fossilized remains of dinoflagellates.[107] Later, cyst formation from gamete fusion was reported, which led to the conclusion that encystment is associated with sexual reproduction.[100] These observations also gave credence to the idea that microalgal encystment is essentially a process whereby zygotes prepare themselves for a dormant period.[108] Because the resting cysts studied until that time came from sexual processes, dormancy was associated with sexuality, a presumption that was maintained for many years. This attribution was coincident with evolutionary theories about the origin of eukaryotic cell fusion and sexuality, which postulated advantages for species with diploid resting stages, in their ability to withstand nutrient stress and mutational UV radiation through recombinational repair, and for those with haploid vegetative stages, as asexual division doubles the number of cells.[104] Nonetheless, certain environmental conditions may limit the advantages of recombination and sexuality,[109] such that in fungi, for example, complex combinations of haploid and diploid cycles have evolved that include asexual and sexual resting stages.[110][103]
However, in the general life cycle of cyst-producing dinoflagellates as outlined in the 1960s and 1970s, resting cysts were assumed to be the fate of sexuality,[100][111] which itself was regarded as a response to stress or unfavorable conditions. Sexuality involves the fusion of haploid gametes from motile planktonic vegetative stages to produce diploidplanozygotes that eventually form cysts, orhypnozygotes, whose germination is subject to bothendogenous andexogenous controls. Endogenously, a species-specific physiological maturation minimum period (dormancy) is mandatory before germination can occur. Thus, hypnozygotes were also referred to as "resting" or "resistant" cysts, in reference to this physiological trait and their capacity following dormancy to remain viable in the sediments for long periods of time. Exogenously, germination is only possible within a window of favorable environmental conditions.[103]
Yet, with the discovery that planozygotes were also able to divide it became apparent that the complexity of dinoflagellate life cycles was greater than originally thought.[112][113] Following corroboration of this behavior in several species, the capacity of dinoflagellate sexual phases to restore the vegetative phase, bypassing cyst formation, became well accepted.[114][115] Further, in 2006 Kremp and Parrow showed the dormant resting cysts of the Baltic cold water dinoflagellatesScrippsiella hangoei andGymnodinium sp. were formed by the direct encystment of haploid vegetative cells, i.e., asexually.[116] In addition, for the zygotic cysts ofPfiesteria piscicida dormancy was not essential.[117][103]
One of the most striking features of dinoflagellates is the large amount of cellular DNA that they contain. Most eukaryotic algae contain on average about 0.54 pg DNA/cell, whereas estimates of dinoflagellate DNA content range from 3–250 pg/cell,[32] corresponding to roughly 3000–215 000 Mb (in comparison, the haploid human genome is 3180 Mb and hexaploidTriticum wheat is 16 000 Mb).Polyploidy or polyteny may account for this large cellular DNA content,[118] but earlier studies of DNA reassociation kinetics and recent genome analyses do not support this hypothesis.[119] Rather, this has been attributed, hypothetically, to the rampant retroposition found in dinoflagellate genomes.[120][121]
In addition to their disproportionately large genomes, dinoflagellate nuclei are unique in their morphology, regulation, and composition. Their DNA is so tightly packed that exactly how many chromosomes they have is still uncertain.[122]
The dinoflagellates share an unusual mitochondrial genome organisation with their relatives, theApicomplexa.[123] Both groups have very reduced mitochondrial genomes (around 6 kilobases (kb) in the Apicomplexa vs ~16kb for human mitochondria). One species,Amoebophrya ceratii, has lost its mitochondrial genome completely, yet still has functional mitochondria.[124] The genes on the dinoflagellate genomes have undergone a number of reorganisations, including massive genome amplification and recombination which have resulted in multiple copies of each gene and gene fragments linked in numerous combinations. Loss of the standard stop codons, trans-splicing of mRNAs for the mRNA of cox3, and extensive RNA editing recoding of most genes has occurred.[125][126] The reasons for this transformation are unknown. In a small group of dinoflagellates, called 'dinotoms' (Durinskia and Kryptoperidinium), the endosymbionts (diatoms) still have mitochondria, making them the only organisms with two evolutionarily distinct mitochondria.[127]
In most of the species, the plastid genome consist of just 14 genes.[128]
The DNA of the plastid in the peridinin-containing dinoflagellates is contained in a series of small circles calledminicircles.[129] Each circle contains one or two polypeptide genes. The genes for these polypeptides are chloroplast-specific because their homologs from other photosynthetic eukaryotes are exclusively encoded in the chloroplast genome. Within each circle is a distinguishable 'core' region. Genes are always in the same orientation with respect to this core region.
In terms ofDNA barcoding, ITS sequences can be used to identify species,[130] where a genetic distance of p≥0.04 can be used to delimit species,[131] which has been successfully applied to resolve long-standing taxonomic confusion as in the case of resolving the Alexandrium tamarense complex into five species.[132] A recent study[133] revealed a substantial proportion of dinoflagellate genes encode for unknown functions, and that these genes could be conserved and lineage-specific.
Dinoflagellates are mainly represented as fossils bydinocysts, which have a long geological record with lowest occurrences during the mid-Triassic,[134] whilst geochemical markers suggest a presence to the Early Cambrian.[135] Some evidence indicates dinosteroids in manyPaleozoic andPrecambrian rocks might be the product of ancestral dinoflagellates (protodinoflagellates).[136][137] Dinoflagellates show a classic radiation of morphologies during the Late Triassic through the MiddleJurassic.[138][139][140] More modern-looking forms proliferate during the later Jurassic andCretaceous.[138] This trend continues into theCenozoic, albeit with some loss of diversity.[138][134]
Molecular phylogenetics show that dinoflagellates are grouped withciliates andapicomplexans (=Sporozoa) in a well-supported clade, thealveolates. The closest relatives to dinokaryotic dinoflagellates appear to beapicomplexans,Perkinsus, Parvilucifera, syndinians, andOxyrrhis.[141] Molecular phylogenies are similar to phylogenies based on morphology.[142][143]
The earliest stages of dinoflagellate evolution appear to be dominated by parasitic lineages, such as perkinsids and syndinians (e.g.Amoebophrya andHematodinium).[144][145][146][147]
All dinoflagellates contain red algal plastids or remnant (nonphotosynthetic) organelles of red algal origin.[148] The parasitic dinoflagellateHematodinium however lacks a plastid entirely.[149] Some groups that have lost the photosynthetic properties of their original red algae plastids has obtained new photosynthetic plastids (chloroplasts) through so-called serial endosymbiosis, both secondary and tertiary:
Lepidodinium unusually possesses a green algae-derived plastid (all other serially-acquired plastids can be traced back to red algae).[150] The plastid is most related to free-livingPedinomonas (hence likely secondary). Two previously undescribed dinoflagellates ("MGD" and "TGD") contain a closely-related plastid.[151]
Karenia,Karlodinium, andTakayama possess plastids ofhaptophyte origin, produced in three separate events.[152]
"Dinotoms" (Durinskia andKryptoperidinium) have plastids derived fromdiatoms.[153][154]
The Kareniaceae (which contains the three haptophyte-having genera) contains two separate cases of kleptoplasty.[156][152]
Dinoflagellate evolution has been summarized into five principal organizational types: prorocentroid, dinophysoid, gonyaulacoid, peridinioid, and gymnodinoid.[157]The transitions of marine species into fresh water have been frequent events during the diversification of dinoflagellates and have occurred recently.[158]
Many dinoflagellates also have a symbiotic relationship with cyanobacteria, called cyanobionts, which have a reduced genome and has not been found outside their hosts. The Dinophysoid dinoflagellates have two genera, Amphisolenia and Triposolenia, that contain intracellular cyanobionts, and four genera; Citharistes, Histioneis, Parahistioneis, and Ornithocercus, that contain extracellular cyanobionts.[159] Most of the cyanobionts are used for nitrogen fixation, not for photosynthesis, but some don't have the ability to fix nitrogen. The dinoflagellateOrnithocercus magnificus is host for symbionts which resides in an extracellular chamber. While it is not fully known how the dinoflagellate benefit from it, it has been suggested it is farming the cyanobacteria in specialized chambers and regularly digest some of them.[160]
^abcFensome RA, Taylor RJ, Norris G, Sarjeant WA, Wharton DI, Williams GL (1993).A classification of living and fossil dinoflagellates. Micropaleontology Special Publication. Vol. 7. Hanover, PA: Sheridan Press.OCLC263894965.
^Müller, O.F. 1773. Vermium terrestrium et fluviatilium, seu Animalium Infusoriorum, Helmithicorum et Testaceorum, non marinorum, succincta historia, vol. 1. Pars prima. p. 34, 135. Faber, Havniae, et Lipsiae 1773.
^Ehrenberg C.G. (1832) Beiträge zur Kenntnis der Organisation der Infusorien und ihrer geographischer Verbreitung, besonders in Sibirien. — Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin. Aus dem Jahre 1830. Physikalische Abhandlungen 1830: 1–88, Pls 1–8.
^Bütschli O. (1885) 3. Unterabtheilung (Ordnung) Dinoflagellata. – In: Dr. H.G. Bronn's Klassen und Ordnungen des Thier-Reichs, wissenschaftlich dargestellt in Wort und Bild. Erster Band Protozoa. – C.F. Winter'sche Verlagshandlung, Leipzig und Heidelberg. Pp. 906–1029; Pl.
^Gaines G, Taylor FJ (May 1985). "Form and function of the dinoflagellate transverse flagellum".J. Protozool.32 (2):290–6.doi:10.1111/j.1550-7408.1985.tb03053.x.
^abCavalier-Smith T (1991). "Cell diversification in heterotrophic flagellates". In Patterson DJ, Larsen J (eds.).The biology of free-living heterotrophic flagellates. Systematics Association Publications. Vol. 45. Clarendon Press. pp. 113–131.ISBN978-0-1985-7747-8.
^abFreudenthal HD (1962). "Symbiodinium gen. Nov. AndSymbiodinium microadriaticum sp. nov., a Zooxanthella: Taxonomy, Life Cycle, and Morphology".The Journal of Protozoology.9 (1):45–52.doi:10.1111/j.1550-7408.1962.tb02579.x.
^Medlin LK, Fensome RA (2013). "Dinoflagellate macroevolution".Biological and Geological Perspectives of Dinoflagellates. Geological Society of London. pp. 263–274.doi:10.1144/tms5.25.ISBN978-1-86239-368-4.
^Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (October 2004). "Dinoflagellates: a remarkable evolutionary experiment".American Journal of Botany.91 (10):1523–1534.doi:10.3732/ajb.91.10.1523.PMID21652307.
^Dodge (1966). Cited but unreferenced inSteidinger KA, Jangen K (1997)."Dinoflagellates". In Tomas CR (ed.).Identifying Marine Phytoplankton. Academic Press. pp. 387–584.ISBN978-0-0805-3442-8.Archived from the original on 2014-07-07. Retrieved2016-03-05.
^Steidinger KA, Jangen K (1997)."Dinoflagellates". In Tomas CR (ed.).Identifying Marine Phytoplankton. Academic Press. pp. 387–584.ISBN978-0-0805-3442-8.Archived from the original on 2014-07-07. Retrieved2016-03-05.
^Schiller, J., 1931–1937: Dinoflagellatae (Peridinineae) in monographischer Behandlung. In: RABENHORST, L. (ed.), Kryptogamen-Flora von Deutschland, Österreichs und der Schweiz. Akad. Verlag., Leipzig. Vol. 10 (3): Teil 1 (1–3) (1931–1933): Teil 2 (1–4)(1935–1937).
^Sournia A (1973). "Catalogue des espèces et taxons infraspécifiques de dinoflagellés marins actuels publiés depuis la révision de J. Schiller. I. Dinoflagellés libres".Beih. Nova Hedwigia.48:1–92.
^Sournia A (1982). "Catalogue des espèces et taxons infraspécifiques de dinoflagellésmarins actuels publiés depuis la révision de J. Schiller. IV. (Complément)".Arch. Protistenkd.126 (2):151–168.doi:10.1016/S0003-9365(82)80046-8.
^Sournia A (1990). "Catalogue des espèces et taxons infraspécifiques de dinoflagellésmarins actuels publiés depuis la révision de J. Schiller. V. (Complément)".Acta Protozool.29:321–346.ISSN0065-1583.
^SOURNIA, A., 1986: Atlas du Phytoplancton Marin. Vol. I: Introduction, Cyanophycées,Dictyochophycées, Dinophycées et Raphidophycées. Editions du CNRS, Paris.
^Steidinger KA, Williams J (1970).Dinoflagellates. Memoirs of the Hourglass Cruises. Vol. 2. Florida: Marine Research Laboratory.OCLC6206528.
^Taylor FJ, Hart-Jones B (1976).Dinoflagellates from the International Indian Ocean Expedition: A Report on Material Collected by the R.V. "Anton Bruun" 1963–1964. Biblioteca Botanica. Vol. 132. E. Schweizerbart.ISBN978-3-5104-8003-6.OCLC3026853.
^Hoppenrath M, Elbrächter M, Drebes G (2009).Marine phytoplankton: selected microphytoplankton species from the North Sea around Helgoland and Sylt. Stuttgart: E. Schweizerbart'sche Verlagsbuchhandlung (Nägele und Obermiller).ISBN978-3-5106-1392-2.
^Schnepf E, Elbrächter M (February 1992). "Nutritional strategies in dinoflagellates: A review with emphasis on cell biological aspects".European Journal of Protistology.28 (1):3–24.doi:10.1016/S0932-4739(11)80315-9.PMID23194978.
^Biecheler B (1952). "Recherches sur les Peridiniens".Bull. Biol. Fr. Belg.36 (Suppl):1–149.ISSN0994-575X.
^abBursa AS (1961). "The annual oceanographic cycle at Igloolik in the Canadian Arctic. II. The phytoplankton".J. Fish. Res. Board Can.18 (4):563–615.doi:10.1139/f61-046.
^Elbrachter M (1979). "On the taxonomy of unarmored dinophytes (Dinophyta) from the Northwest African upwelling region".Meteor Forschungsergebnisse.30:1–22.
^Frey LC, Stoermer EF (1980). "Dinoflagellate phagotrophy in the upper Great Lakes".Trans. Am. Microsc. Soc.99 (4):439–444.doi:10.2307/3225654.JSTOR3225654.
^Cachon PJ, Cachon M. "Le systeme stomatopharyngien de Kofoidinium Pavillard. Comparisons avec celui divers Peridiniens fibres et parasites".Protistologica.10:217–222.
^Gaines G, Taylor FJ (1984). "Extracellular digestion in marine dinoflagellates".J. Plankton Res.6 (6):1057–61.doi:10.1093/plankt/6.6.1057.
^Adolf JE, Krupatkina D, Bachvaroff T, Place AR (2007). "Karlotoxin mediates grazing byOxyrrhis marina on strains ofKarlodinium veneficum".Harmful Algae.6 (3):400–412.Bibcode:2007HAlga...6..400A.doi:10.1016/j.hal.2006.12.003.
^Schütt F (1895). "2. Teil, Studien über die Zellen der Peridineen".Die Peridineen der Plankton-Expedition. Ergebnisse der Plankton-Expedition der Humboldt-Stiftung. Allgemeiner Theil. pp. 1–170.OCLC69377189.
^Schlüter L, Møhlenberg F, Havskum H, Larsen S (2000). "The use of phytoplankton pigments for identifying and quantifying phytoplankton groups in coastal areas:testing the influence of light and nutrients on pigment/chlorophyll a ratios".Marine Ecology Progress Series.192:49–63.Bibcode:2000MEPS..192...49S.doi:10.3354/meps192049.ISSN0171-8630.S2CID56561696.
^Faust M, Gulledge, R.A. (2002).Identifying Harmful Marine Dinoflagellates. Contributions from the United States National Herbarium. Vol. 42. Washington, D.C.: Department of Systematic Biology, Botany, National Museum of Natural History.ISSN0097-1618. Archived fromthe original on 2007-04-30. Retrieved2007-05-18.
^Poupin, J., A.-S. Cussatlegras, and P. Geistdoerfer. 1999. Plancton marin bioluminescent. Rapport scientifique du Laboratoire d'Océanographie de l'École Navale LOEN, Brest, France, 83 pp.
^Sweeney B.Bioluminescence and circadian rhythms. In:Taylor 1987, pp. 269–281
^Knaust R, Urbig T, Li L, Taylor W, Hastings JW (February 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".J. Phycol.34 (1):167–172.Bibcode:1998JPcgy..34..167K.doi:10.1046/j.1529-8817.1998.340167.x.S2CID84990824.
^Fritz L, Morse D, Hastings JW (February 1990). "The circadian bioluminescence rhythm of Gonyaulax is related to daily variations in the number of light-emitting organelles".Journal of Cell Science.95 (Pt 2):321–328.doi:10.1242/jcs.95.2.321.PMID2196272.
^Reinsch, P.F. (1905) "Die palinosphärien, ein mikroskopischer vegetabile organismus in der mukronatenkreide". ..Cent. Miner. Geol. Palaeontol..., 402–407.
^Uchida T, Matsuyama Y, Yamaguchi M, Honjo T (1996). "The life cycle of Gyrodinium instriatum (Dinophyceae) in culture".Phycological Research.44 (3):119–123.doi:10.1111/j.1440-1835.1996.tb00040.x.S2CID84051080.
^Lin S, Zhang H, Spencer DF, Norman JE, Gray MW (July 2002). "Widespread and extensive editing of mitochondrial mRNAS in dinoflagellates".Journal of Molecular Biology.320 (4):727–739.doi:10.1016/S0022-2836(02)00468-0.PMID12095251.
^Moldowan JM, Dahl JE, Jacobson SR, Huizinga BJ, Fago FJ, Shetty R, et al. (February 1996). "Chemostratigraphic reconstruction of biofacies: molecular evidence linking cyst-forming dinoflagellates with Pre-Triassic ancestors".Geology.24 (2):159–162.Bibcode:1996Geo....24..159M.doi:10.1130/0091-7613(1996)024<0159:CROBME>2.3.CO;2.
^Talyzina NM, Moldowan JM, Johannisson A, Fago FJ (January 2000). "Affinities of early Cambrian acritarchs studied by using microscopy, fluorescence flow cytometry and biomarkers".Rev. Palaeobot. Palynol.108 (1–2):37–53.Bibcode:2000RPaPa.108...37T.doi:10.1016/S0034-6667(99)00032-9.
^Gunderson JH, Goss SH, Coats DW (1999). "The phylogenetic position of Amoebophrya sp. infecting Gymnodinium sanguineum".The Journal of Eukaryotic Microbiology.46 (2):194–197.doi:10.1111/j.1550-7408.1999.tb04603.x.PMID10361739.S2CID7836479. Gunderson JH, John SA, Boman WC, Coats DW (2002). "Multiple strains of the parasitic dinoflagellate Amoebophrya exist in Chesapeake Bay".The Journal of Eukaryotic Microbiology.49 (6):469–474.doi:10.1111/j.1550-7408.2002.tb00230.x.PMID12503682.S2CID30051291.
^Kretschmann J, Žerdoner Čalasan A, Gottschling M (January 2018). "Molecular phylogenetics of dinophytes harboring diatoms as endosymbionts (Kryptoperidiniaceae, Peridiniales), with evolutionary interpretations and a focus on the identity of Durinskia oculata from Prague".Molecular Phylogenetics and Evolution.118:392–402.Bibcode:2018MolPE.118..392K.doi:10.1016/j.ympev.2017.10.011.PMID29066288.
^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 preyMesodinium Rubrum. Journal of Phycology, 48: 569-579. doi:10.1111/j.1529-8817.2012.01150.x
^Mertens KN, Takano Y, Head MJ, Matsuoka K (2014). "Living fossils in the Indo-Pacific warm pool: A refuge for thermophilic dinoflagellates during glaciations".Geology.42 (6):531–534.Bibcode:2014Geo....42..531M.doi:10.1130/G35456.1.
^Montresor M, Janofske D, Willems H (1997). "The cyst-theca relationship inCalciodinellum operosum emend. (Peridiniales, Dinophyceae) and a new approach for the study of calcareous cysts".Journal of Phycology.33 (1):122–131.Bibcode:1997JPcgy..33..122M.doi:10.1111/j.0022-3646.1997.00122.x.S2CID84169394.
^Gu H, Kirsch M, Zinssmeister C, Soehner S, Meier KJ, Liu T, et al. (September 2013). "Waking the dead: morphological and molecular characterization of extant †Posoniella tricarinelloides (Thoracosphaeraceae, Dinophyceae)".Protist.164 (5):583–597.doi:10.1016/j.protis.2013.06.001.PMID23850812.
_by_Noctiluca_in_Nagasaki.jpg)
Material was copied from this source, which is available under aCreative Commons Attribution 3.0 International LicenseArchived 2011-02-23 at theWayback Machine.
