Phycology - Kostikov, I.Y. - 2009-2013

Chapter 19. Dinoflagellates – Dinophyta

The division Dinophyta comprises approximately 2,000 extant species. About 2,000 species are also known in the fossil record. The earliest remains of dinoflagellates are predominantly represented by cysts (the so-called hystrichospheres), found in Silurian (435–460 million years ago) and Precambrian (600 million years) sedimentary rocks. Dinoflagellates dominated as primary producers during the Paleozoic era, the Jurassic–Cretaceous periods (180–100 million years ago), and the Eocene (60–50 million years) of the Mesozoic era.

Extant dinoflagellates predominantly inhabit marine plankton, while a small number of species (around 200) are distributed in continental freshwaters and hypersaline Water bodies. Some representatives develop in massive quantities on snow and ice. Certain Dinophyta parasitize marine Arthropods, polychaetes (ellobiofycids), various other marine animals (syndinofycids), or form symbiotic associations with coral polyps.

Almost all dinoflagellates are microscopic organisms, ranging in size from 6 to 1500 µm (with an average of 30–60 µm). The vast majority of Dinophyta possess a flagellate (monad) Structure.

Dinoflagellates represent a distinct Lineage of tubular-cristate eukaryotes, which, together with Ciliates and apicomplexans, form a separate phylum – the alveolates.

Class="center">Taxonomic CHARACTERISTICS OF THE division

Pigments and reserve nutrients

In Dinophyta, the pigment composition is not a universal taxonomic character. Approximately 50% of species are obligate heterotrophs and lack Photosynthetic Pigments. Among photoautotrophic representatives, at least four different pigment combinations are currently known: the first is considered primary, while the others are secondary.

The primary pigment combination is characteristic of the vast majority of photoautotrophic dinoflagellates. It includes chlorophylls a and c, β-carotene, and the xanthophylls peridinin, diadinoxanthin, and dinoxanthin. METABOLISM/14.html">Chloroplasts in representatives with the primary combination are colored in various shades of yellow.

The second combination is represented by chlorophylls a and b, along with β- and, likely, γ-carotenes. Algae possessing this pigment combination are green in color.

The third and fourth pigment combinations are represented by chlorophylls a and c, β-carotene, and the xanthophyll fucoxanthin or neofucoxanthin, as well as diadinoxanthin and diatoxanthin. In addition, the fourth combination also contains phycobilin pigments – phycocyanin and phycoerythrin. The chloroplasts of representatives with the third combination are yellow or brown, while those with the fourth are red or blue-green.

Various combinations of pigments are due to the presence of chloroplasts of different evolutionary origins: in algae with the primary pigment combination, chloroplasts originate from green algae of the class Prasinophyceae, whereas in those with secondary combinations, they derive from both prasinophytes and golden or cryptophyte algae.

The assimilation products are starch and oil, more rarely chrysolaminarin, and Glycogen in obligately heterotrophic species. All assimilates are stored outside the chloroplasts. In algae with the fourth pigment combination, starch may also be deposited in the periplastidal space.

Cytological Characteristics

Cell Coverings. Dinoflagellates possess a distinctive, unique type of covering known as the amphiesma, located beneath the Plasmalemma. The amphiesma consists of a layer of tightly appressed, flattened membranous vesicles. The number of vesicles varies among different taxa, ranging from two to several dozen. These vesicles are either filled with a granular matrix or contain a polysaccharide (likely cellulosic) plate deposited within each vesicle. In the former case, the amphiesma is elastic, the Cells are capable of slight metabolic changes in shape, and they disintegrate upon fixation with formaldehyde. Algae with this type of amphiesma are sometimes erroneously referred to as "naked".

If plates are formed within the vesicles, the cells maintain a fixed shape, are non-metabolic, and do not collapse during fixation. This variant of the amphiesma is termed a theca. The surface of the armored plates is typically intricately ornamented, featuring polygonal segments perforated by one or several pores. In many species, trichocysts are situated beneath these pores.

Trichocysts are flask-shaped capsules attached by their neck to the amphiesma directly beneath a pore. The capsule is bounded by a Plasma Membrane and contains a tightly packed, cross-striated thread folded in a hexagonal pattern. Upon cell irritation, the thread is discharged explosively through the pore. Representatives of the genera Nematodinium and Polykrikos have been found to possess nematocysts similar to the ejection structures of Cnidarians.

Interestingly, in some dinoflagellates, a layer of submicroscopic organic scales is also present above the amphiesma On the surface of the plasmalemma. These scales are synthesized in the Golgi apparatus, subsequently transported to The Cell surface, and deposited on the plasmalemma.

Occasionally, the cell coverings are represented solely by the plasmalemma (e.g., in Dinamoebidium), in which case the cells exhibit an amoeboid structure and are capable of forming various types of pseudopodia.

In non-motile (hemimonadoid, coccoid, and filamentous) dinoflagellates, the cells are enveloped by a true cellulosic-pectinic wall.

General Cell Architecture. The cells are predominantly dorsoventrally flattened. A characteristic feature is the presence of two furrows: a transverse and a longitudinal one. In the region of the furrows, the amphiesma is absent, and the protoplast is separated from the external environment solely by the plasmalemma. The longitudinal furrow is located on the ventral side and is intersected by the transverse furrow. The latter divides the cell into an upper part, the epicone, and a lower part, the hypocone. Two heterokont, heteromorphic, and heterodynamic flagella emerge from the junction of the furrows. One flagellum lies in the transverse furrow and serves for propulsion, while the other lies in the longitudinal furrow and Functions as a rudder.

Near the flagellar bases lies the vacuolar apparatus, represented by non-pulsating vacuoles known as pusules. A pusule is a deep, branched cavity formed by an invagination of the plasmalemma. The cavity communicates with the external environment via a short, narrow canal.

In the region of the longitudinal furrow, the cells of certain species form pseudopodia, which they use to actively capture food particles (primarily diatom cells). Digestion of the prey takes place within digestive vacuoles.

Four types of eyespots (stigmata) have been discovered in dinoflagellates. The first type of eyespot consists of several spherical globules located directly in the Cytoplasm. The second type comprises a single row of small globules situated within the chloroplast stroma. The third type of eyespot consists of several parallel rows of pigment globules surrounded by a triple plasma membrane, which is adjacent to the so-called lamellar body. The latter is formed by a system of parallel, flattened membranous vesicles, with the marginal vesicles transitioning into the channels of The Endoplasmic reticulum.

The type 4 stigma is a complex structure that somewhat resembles an eye in its Organization. Located in the cytoplasm and surrounded by a ring of Mitochondria, it consists of a lens-like body and a single layer of pigment globules, with a specialized structure known as the retinoid situated between them.

Nuclear apparatus. In the vast majority of dinoflagellates, The Nucleus differs significantly from typical eukaryotic nuclei. These differences stem from the fact that Chromosomes are almost entirely devoid of Histones (the histone-to-DNA ratio in a typical dinoflagellate nucleus averages 0.04 : 1, compared to 1 : 1 in a typical eukaryotic nucleus). Consequently, the thickness of Chromatin microfibrils is approximately ten times smaller than in other eukaryotes (2 nm versus 25 nm, respectively). Throughout the entire Cell Cycle, chromosomes remain in a hyper-supercoiled state, forming characteristic chromatin garlands. The chromosomes are attached to the nuclear envelope via centromeres.

Nuclear division in Dinophyta is equally unique. Prior to division, DNA Replication takes place, with each chromatid possessing its own kinetochore that attaches it to the nuclear envelope. At the onset of division, cytoplasmic tunnels form within the nucleus, into which bundles of microtubules plunge. Most of these microtubules pass all the way through the tunnels, forming an interzonal spindle. Individual isolated microtubules attach to the chromatid kinetochores. The elongation of these interzonal microtubules drives the stretching of the nucleus and the Separation of sister kinetochores along with their chromatids. Thus, the nuclear envelope remains intact during division, making mitosis closed and acentric.

A peculiar nuclear behavior occurs during Meiosis: in prophase, the nucleus begins to rotate at a speed of 2 rpm, facilitating chromosome conjugation and Crossing-over. This phenomenon is known as cyclosis, and its observation serves as an indicator of the onset of reductional division.

Until recently, the nuclear apparatus and nuclear division of dinoflagellates—which resembled simple pinching under a Light Microscope—were considered primitive. For this reason, the nucleus in Dinophyta was termed mesokaryotic, meaning it was viewed as transitional between the prokaryotic nucleoid and a true eukaryotic nucleus.

However, molecular phylogenetic studies, later corroborated by Electron Microscopy, demonstrated that the so-called mesokaryotic nucleus is not an intermediate state, but rather derived from a true eukaryotic nucleus. It was also established that in primitive dinoflagellates (such as Oxyrrhis), the nucleus exhibits the normal chromosomal organization and typical mitosis characteristic of other eukaryotes. Furthermore, it was discovered that vegetative cells in moderately advanced dinoflagellates (specifically of the genus Noctiluca) possess a typical eukaryotic nucleus, whereas their Gametes feature the typical dinoflagellate "mesokaryotic" nucleus. Consequently, in modern literature, the typical dinoflagellate nucleus is referred to not as mesokaryotic, but as dinokaryotic, or a dinokaryon.

Photosynthetic apparatus. Similar to their pigment composition, the chloroplasts in photoautotrophic Dinophyta occur in four variants:         the primary

(dinophyte) type and at least three additional types—namely, the chlorophyte, chrysophyte, and cryptophyte types.

The primary-type chloroplast is bounded by three membranes. The two inner membranes constitute the chloroplast envelope proper, while the outer membrane is derived from the endoplasmic reticulum. Thylakoids are grouped in threes, and girdle thylakoids are absent. Primary-type chloroplasts contain the primary pigment combination. Based on molecular studies of chloroplast DNA, it is hypothesized that this chloroplast type arose through the endosymbiosis of heterotrophic dinoflagellates with prasinophyte algae (Chlorophyta) containing chlorophylls a and c.

Chloroplasts of the second type (the chlorophyte type) are bounded by four membranes. The two inner membranes represent the chloroplast envelope proper. The first outer membrane is a modified plasmalemma of the originally heterotrophic dinoflagellate, likely originating from a food vacuole membrane. The second outer membrane is the plasmalemma of the chloroplast precursor endosymbiont. Between the inner and outer membranes lies the periplastidial space, which houses a specialized nucleus-like organelle called a nucleomorph. Bounded by a double-membrane envelope, the nucleomorph contains its own DNA. Thylakoids within the chloroplast stroma are likewise grouped in threes. The pigment composition of second-type chloroplasts corresponds to the second combination.

The results of molecular phylogenetic research, comparative biochemical analyses, and ultrastructural studies indicate that this second-type plastid originated from the endosymbiosis of a primarily heterotrophic dinoflagellate with a photoautotrophic green alga (preliminarily identified as also belonging to the Prasinophyceae). Moreover, the nucleomorph represents the vestigial Nucleus of the endosymbiont cell.

Chloroplasts of the third type (the chrysophyte type) are enveloped by five membranes. The two inner membranes form the chloroplast envelope proper, the third and fourth constitute the chloroplast endoplasmic reticulum, and the fifth (outer) membrane is referred to as the perisymbiotic membrane. Thylakoids are grouped in threes, and a triple-thylakoid girdle lamella runs along the peripheral layer of the chloroplast stroma. Chloroplasts of this type possess the third pigment combination.

The space between the second and third membranes represents the periplastidial space of the algal endosymbiont, while that between the fourth and fifth membranes corresponds to the vestigial cytoplasm of the endosymbiont. The Origin of the fifth (perisymbiotic) membrane remains a matter of debate: some authors view it as a modified food vacuole membrane of the host cell, whereas others suggest it is formed by the plasmalemma of the endosymbiont. The endosymbiont that gave rise to the chrysophyte-type plastid is believed to be a golden alga.

Chloroplasts of the fourth—cryptophyte—type possess the most complex structure. They are also enveloped by five membranes: two chloroplast envelope membranes, two chloroplast endoplasmic reticulum membranes, and an outer perisymbiotic membrane. Thylakoids in the chloroplast stroma are grouped in pairs and bear phycobilin pigments on their opposing sides. Girdle thylakoids are absent. The periplastidial space between the second and third membranes contains Ribosomes, starch granules, and membranous cisternae. A nucleomorph is absent. The space between the fourth and fifth membranes—the vestigial cytoplasm of the endosymbiont—contains mitochondria with lamellar (!) cristae, reduced smooth and rough endoplasmic reticulum, cisternae and vesicles, and ribosomes. Remnants of the endosymbiont nucleus have not been detected within this vestigial cytoplasm. A comprehensive array of diverse features indicates that the endosymbiont giving rise to the fourth-type plastid was a cryptophyte alga.

Mitochondria of dinoflagellates feature tubular cristae. Interestingly, dinoflagellates with fourth-type chloroplasts possess two distinct types of mitochondria: firstly, cytoplasmic mitochondria with tubular cristae, and secondly, mitochondria with lamellar cristae located within the vestigial cytoplasm of the endosymbiont—situated between the outer membrane of the chloroplast Endoplasmic reticulum and the perisymbiotic membrane of the chloroplast.

Flagellar apparatus. Motile cells of dinoflagellates possess two heterokont, heteromorphic, and heterodynamic flagella. They emerge from small depressions known as flagellar canals, typically located on the ventral side of the cell at the intersection of the longitudinal and transverse sulci. One flagellum—the transverse flagellum—is directed to the right and lies within the transverse sulcus, while the second—the longitudinal flagellum—is oriented toward the hypocone and rests in the longitudinal sulcus.

The transverse flagellum performs a locomotor function. It appears as a undulating ribbon resembling the undulating membrane of trypanosomes. A striated fiber composed of the protein centrin runs through the central region of the flagellum, surrounded by a spiraling axoneme. In some species, the axoneme conforms to the typical eukaryotic 9+2 formula, whereas in many others it is reinforced with additional microtubules and described by the formula 9+9+2 or 9+3. The flagellar surface bears a single row of simple mastigonemes that are slightly expanded at the base. Much like in stramenopiles, these mastigonemes are assembled within endoplasmic reticulum cisternae, yet they lack a tripartite structure. Near its base within the flagellar canal, the transverse flagellum features a Swelling known as the paraxial body, which acts as a photoreceptor; THE POSITION OF the stigma is usually coordinated with this structure.

The longitudinal flagellum functions as a rudder. It is somewhat flattened, with an axoneme corresponding to the 9+2 formula. The surface of the longitudinal flagellum bears 1 to 3 rows of simple mastigonemes.

The transition zone is identical in both flagella: directly beneath the central microtubules lie two parallel discs, below which some species feature one or several rings, occasionally followed further down by a short helical structure.

Extending from the basal body of the longitudinal flagellum toward the hypocone is a single microtubular ROOT consisting of 10–30 microtubules. The basal body of the transverse flagellum is connected to a striated microfibrillar root directed toward the epicone. Both roots are linked by a striated bridging fiber. A short striated collar extends from each root, wrapping around the lower portion of each basal body. Additionally, a connecting "nuclear" fiber known as the rhizoplast associates with the microtubular root, linking the flagellar root system to the nuclear envelope.

In certain dinoflagellates (such as members of the genus Prorocentrum), the flagella are nearly identical, and the transverse sulcus is reduced to an apical depression. In isolated species, the longitudinal flagellum is reduced, although its basal body and microtubular root are retained.

Feeding characteristics. Dinoflagellates exhibit two widespread nutritional modes: photoautotrophic and heterotrophic. Approximately half of all Dinophyta species are pigmented forms possessing chloroplasts and capable of oxygenic Photosynthesis. Other representatives of this division are colorless and obligate heterotrophs.

Heterotrophic Dinophyta can consume organic matter dissolved in water via an osmotrophic pathway, absorbing it across their entire body surface. However, the primary mode of organic nutrient acquisition is phagotrophy.

The capture of food particles is carried out using specialized pseudopodia formed on the ventral side of the cell in the region of the longitudinal sulcus. These pseudopodia contain bundles of microtubules arranged in a basket-like formation. Through the elongation of these microtubules, the pseudopodia extend and engulf the prey (most commonly planktonic green, golden, or diatom algae). Once the prey enters the basket, its apex closes, and a large food vacuole forms around the captured Organism.

These pseudopodia can exceed the size of the dinoflagellate cell itself several times over, enabling the predator to capture prey much larger than itself. For instance, Gymnodinium fungiforme has cells measuring about 15 µm in diameter, yet it captures ciliates ranging from 0.5 to 1 mm in length.

In parasitic dinophytes (for example, in the freshwater photoautotrophic alga Stylodinium), a pseudopodium penetrates the cells of large filamentous algae, subsequently capturing a portion of the victim's cytoplasm and drawing it into its own cell. In this process, the cytoplasmic matrix components are digested first, whereas membranous Organelles (primarily chloroplasts) remain in the digestive vacuole for some time. Consequently, one can occasionally observe Two Types of chloroplasts simultaneously within the cytoplasm of Stylodinium: the alga's own golden chloroplasts and the green chloroplasts of its prey.

It is believed that heterotrophic Dinophyta acquired their chloroplasts in a similar manner.

Body Plans

The phylum features algae representing four types of morphological body structure. The vast majority of species are planktonic unicellular monadoid organisms. Approximately 10% of species possess an amoeboid structure. There is also a small group of dinophyte algae characterized by hemimonadoid, coccoid, and filamentous types of morphological structure.

Reproduction and Life Cycles

Dinophyte algae reproduce predominantly asexually, while a sexual process has been documented in about 50 species.

The primary mode of asexual reproduction is vegetative Cell Division by binary fission. In unarmored species, daughter cells inherit either the epicone or hypocone amphiesma from the mother cell and subsequently synthesize the missing half. A significant portion of armored species shed their amphiesma prior to division, after which the daughter cells develop a completely new armor. Asexual reproduction via zoospores is also quite common. Some species additionally form aplanospores.

The sexual process occurs via iso- or heterogamy; in certain species, vegetative cells function as gametes, making the process essentially analogous to hologamy. Gametes may be naked or enclosed in a robust amphiesma. In the latter case, gametes copulate by fusing along their ventral sides, whereupon the ventral plates dissolve and the nucleus of the male gamete passes into the female gamete.

Following copulation, a motile planzygote is formed. Its germination proceeds via one of four pathways.

1. Noctiluca: vegetative cell - R! - isogametes - planzygote (rapidly germinating into a vegetative cell). Diplophasic cycle with gametic reduction.

2. Amphidinium: vegetative cells - copulation - zygote (skipping the planzygote stage) - resting period - R! - vegetative cells. Haplophasic cycle with zygotic reduction and no planzygote stage.

3. Ceratium horridum: vegetative cell - micro- and macrogametes - planzygote (extended duration) - R! - vegetative cells. Haplophasic cycle with zygotic reduction and an extended planzygote stage.

4. Ceratium cornutum: two types of vegetative cells (A-cells and a-cells) - two types of micro- and macrogametes (A and a microgametes, A and a macrogametes) - copulation - triflagellated planzygote - hypnozygote - resting period - naked prevégetative cell (sporophyte?) - R! - vegetative cells (two of A-type, two of a-type). Haplodiplophasic cycle with sporic reduction, heteromorphic Morphology/12.html">ALTERNATION OF GENERATIONS, and an extended planzygote stage.

5. Gymnodinium pseudopalustre: vegetative cell - gametes - planzygote (extended duration) - hypnozygote - resting period - prevégetative cell (sporophyte) - R! - zoospores - vegetative cells. Haplodiplophasic cycle with sporic reduction, isomorphic alternation of generations, and an extended planzygote stage.

Thus, Dinophyta exhibit haplophasic, primitive haplodiplophasic, and diplophasic life cycles, with chromosome number reduction being zygotic, sporic, or gametic.

Taxonomic System of the Phylum

Similar to most other algal phyla, a considerable variety of taxonomic systems for Dinophyta exist today. Based on their underlying principles, they can be divided into morphological (classical) and synthetic systems.

Classical Systems

These systems are primarily founded on the morphological Features of the cells—The structure of coverings, presence of a girdle (transverse sulcus), position and orientation of flagella, type of morphological body structure, and lifestyle (free-living or parasitic). The morphological approach was developed during the 1920s–1970s, with the system proposed by J.D. Dodge and its various modifications gaining the widest acceptance and recognition¹.

According to the morphological system, the phylum is divided into two classes: Desmophyceae and Dinophyceae.

Class Desmophyceae encompasses algae with a monadoid structure lacking a transverse sulcus; the flagella are located at the anterior end of the cell, and the amphiesma consists of only two vesicles that join longitudinally to form a suture.

Based on structural types and The ability to form armor, the class is divided into three orders: Desmomastigales, Prorocentrales, Desmocapsales.

Class Dinophyceae unites algae with monadoid, hemimonadoid, coccoid, and filamentous structures (with monadoid representatives predominating). Monadoid cells possess longitudinal and transverse sulci, as well as longitudinal and transverse flagella originating on the ventral side of the cell. The amphiesma consists of numerous vesicles and frequently forms armor. Based on morphological structure types, covering organization, and certain ecological traits, the class is divided into 8 orders: Gymnodiniales, Peridiniales, Dinophysidales, Blastodiniales, Dinamoebidiales, Gloeodiniales, Dinococcales, Dinotrichales.

Synthetic (Molecular-Cytological) System

The system of the phylum is based on molecular phylogeny data, primarily analyses of molecular phylogenetic trees derived from nucleotide sequences of the ribosomal RNA Gene. The phylum's structural framework follows the Dinophyta Classification by R.A. Fensome et al. (1993), as modified by G.W. Saunders et al. (1997).

The division includes five distinct lineages regarded as taxonomic classes: Oxyrrhidophyceae, Syndiniophyceae, Noctiluciphyceae, Blastodiniphyceae, and Dinophyceae. These lineages correlate well with the ecological traits and cytological features of their representatives, particularly nuclear structure, nuclear division, and the architecture of the flagellar apparatus. All classes except Dinophyceae are monotypic and comprise a single order.

Class Oxyrrhidophyceae

Represented solely by the genus Oxyrrhis. This alga inhabits marine environments and coastal lagoons, and is quite frequently found in the coastal waters of the Black and Azov seas.

Oxyrrhis possesses two isokont, isomorphic, and isodynamic flagella, both of which correspond in structure to the longitudinal flagellum of "typical" dinoflagellates (Fig.). The nucleus has a typical eukaryotic structure; during interphase, the chromatin is despiralized, and nuclear DNA is bound to histones, meaning it is organized according to the standard eukaryotic plan. The mitotic spindle is intranuclear. The alga is colorless and exhibits osmotrophic Nutrition.

Class Syndiniophyceae

Unites highly specialized intracellular parasitic algae characterized by an amoeboid structure and a eukaryotic nucleus. Syndiniophyceans retain certain features of "typical" dinoflagellates: for instance, their monad stages possess a transverse flagellum with a characteristic "dinoflagellate" structure, and the mitotic spindle forms extranuclearly within cytoplasmic tunnels passing through the nucleus. All Syndiniophyceans are obligate heterotrophs, with phagotrophy being the predominant mode of nutrition. Food is captured by pseudopodia, which, however, lack microtubular baskets.

Syndiniophyceans parasitize the cells of marine ciliates, crustaceans, fish, and large "true" dinoflagellate algae.

Class Noctiluciphyceae

Includes obligately heterotrophic, free-living marine algae, with the genus Noctiluca being a characteristic representative.

This alga feeds phagotrophically, capturing food particles with a tentacle that contains microtubular supporting elements. The latter somewhat resemble a microtubular basket. Vegetative cells are large (up to 1 mm in diameter), possess only a single flagellum corresponding in structure to a typical longitudinal flagellum, and contain a large vacuole traversed by cytoplasmic strands. The cells are covered by an amphiesma whose vesicles are fluid-filled and lack plates. The cell contains a single nucleus with a diploid set of chromosomes organized according to the eukaryotic scheme: interphase chromatin is despiralized, and DNA is bound to histones. Mitosis is also of the eukaryotic type, yet it is carried out using the extranuclear spindle characteristic of dinoflagellates.

Monad stages are represented by gametes that form within the vegetative cell following reduction division. Unlike vegetative cells, these gametes possess a dinokaryotic nucleus with spiralized interphase chromosomes that are not bound to histones. The flagellar apparatus of the gametes is of the typical dinoflagellate structure, with the longitudinal and transverse flagella emerging from the intersection of the longitudinal and transverse sulci.

Notable features of Noctiluca include, firstly, the ability for Bioluminescence, and secondly, The formation of symbioses with small unicellular green algae. Due to the latter, some populations of Noctiluca effectively transition to autotrophic nutrition.

Noctiluca is considered a cosmopolitan alga found in the seas of the temperate, subtropical, and tropical zones.

Class Blastodiniphyceae

Unites algae that are intratissue parasites of aquatic animals, predominantly from the crustacean class (Crustacea). The monad cells of blastodiniphyceans possess a genuine dinokaryotic nuclear apparatus. In vegetative trophocytes and gonocytes, mitosis is typically dinoflagellate. The vast majority of representatives possess true chloroplasts of the primary type. Only a single species is colorless and feeds exclusively heterotrophically. Thus, almost all species of the class exhibit mixotrophic nutrition.

A characteristic representative is Blastodinium spinulosum. This alga parasitizes the cuticular layer of the Digestive System of copepods (order Copepoda) and features a specialized developmental cycle comprising trophocyte, gonocyte, zoospore (sporocyte), and cyst stages.

The young trophocyte develops among the host's intestinal cells. It is elongated, bears a transverse sulcus that encircles the cell twice, and is covered by a soft amphiesma devoid of plates. The center of the cell contains a nucleus that appears eukaryotic under light microscopy. Several small yellow chloroplasts are located at the periphery. Flagella are absent. The adult trophocyte divides into two or three cells, one of which transforms into a gonocyte, while the others give rise to new trophocytes.

The gonocyte divides rapidly, producing numerous zoospores—sporocytes. Sporocytes exhibit a structure typical of Dinophyta: longitudinal and transverse sulci, two heteromorphic flagella, a dinokaryon, and chloroplasts. The sporocytes leave the host's body through the anus and subsequently encyst. When the cyst is swallowed by another crustacean, a young cell emerges, penetrates the Tissues of the intestinal cuticular layer, and transforms into a new trophocyte.

Class Dinophyceae

The principal diagnostic feature of the class is the presence of a dinokaryon and typically dinoflagellate mitosis across all stages of The life cycle. The vast majority of dinophyceans are monadal algae with a typical dinoflagellate cellular plan—longitudinal and transverse sulci, cellular differentiation into an epitheca and hypotheca, two heteromorphic flagella—and are capable of phagotrophic nutrition, wherein prey is captured by pseudopodia possessing microtubular baskets. Eugamic dinophyceans exhibit a haplophasic life cycle. Dinophyceans lead a predominantly free-living lifestyle, less frequently acting as intratissue or intracellular symbionts of animals and algae. Some are de facto unicellular "herbivorous" consumers. The class is divided into five orders—Amphidiniales, Goniaulacales, Symbiodiniales, Peridiniales, and Prorocentrales (Table 10.3.1)—among which the latter two are dominant.

Amphidiniales unites monadal algae with a soft amphiesma that does not form a theca. The transverse sulcus in amphidinialeans is displaced toward the apex of the cell. Cytological features of the order include the formation of a small number of tunnels (2–4) during mitosis, and a relatively low number of chromosomes in the interphase nucleus—ranging from 24 to 36. Under unfavorable conditions, cells transform into spherical cysts surrounded by a layer of mucus. Based on molecular data, Amphidiniales is the most ancient order of the class. A characteristic representative is the genus Amphidinium, species of which inhabit primarily marine plankton.

Sexual reproduction is known in certain species of this genus (specifically, Amphidinium carteri). Unlike dinophyceans from other orders, the zygote lacks a prolonged motile planzygote stage; immediately following copulation, it loses its flagella, rounds off, and transforms into a resting hypnozygote.

Goniaulacales includes dinophycean algae covered by a robust theca and possessing a specific type of cell division: daughter cells inherit half of the amphiesma from the mother cell and independently synthesize only the missing portion. Consequently, chains of cells frequently form, especially in culture. The assumption that such division in dinophyceans represents a primitive trait is well supported by the results of molecular phylogenetic reconstructions. An additional feature of the order is the presence of a long longitudinal sulcus that typically extends onto the epitheca, reaching the cell apex. Representatives of Goniaulacales are also characterized by a high chromosome count—ranging from 100 to 300.

Eugamic species of the order possess a specialized type of gamete copulation: a microgamete enters the cytoplasm of a macrogamete through an opening located on the latter's ventral side. The thecal plate of the macrogamete in the region of this opening disintegrates prior to copulation. The theca of the microgamete gradually dissolves within the cytoplasm of the macrogamete; after some time, only the nucleus of the male gamete remains in the cytoplasm. Later, it fuses with the nucleus of the macrogamete. Thus, the gametes do not fuse in the conventional sense; rather, the female gamete "devours" the male.

Life cycles are haplophasic or haplodiplophasic, featuring a prolonged motile planzygote stage.

Characteristic representatives of the order are the genera Goniaulax and Ceratium, species of which typically inhabit marine plankton, with only occasional representatives found in fresh continental waters.

Morphologically, these genera are easily distinguished from one another: Goniaulax cells are more or less ellipsoidal, and the theca does not form prominent outgrowths. In Ceratium, the theca forms three or four large horns—one on the epicone and two or three on the hypocone.

Symbiodiniales (Suessiales) represent a specific group of dinoflagellates that are endosymbionts of coral-building cnidarians. A characteristic representative of the order is the genus Symbiodinium.

The vegetative cells of Symbiodinium—zooxanthellae—lack flagella, contain several yellow or brown chloroplasts, and possess a dinokaryon with a low number of chromosomes (typically 4 to 10). Zooxanthellae reside in the cytoplasm of the host cells and supply the latter with low-molecular-weight metabolites produced during photosynthesis (glycerol, glucose, Alanine, glycolate). In return, the alga receives nitrogen from the polyp in the form of ammonium or urea.

Typically, zooxanthellae divide within the host's endodermal cells and are transmitted to young polyps within eggs.

If the number of zooxanthellae in a polyp cell becomes too high, the alga enters a cyst state. Along with undigested remains, some cysts are pushed out into the gastrovascular cavity and subsequently into the external environment. There, a monad cell of typical dinoflagellate structure or two to four aplanospores emerge from the cyst. The latter also germinate into monad cells. During the polyp's feeding process, these cells enter the gastral cavity, where they are engulfed by the endodermal cells. Inside the latter, they continue their development as zooxanthellae.

Peridiniales is the most species-rich order of the class. It unites representatives with various types of morphological structures—monadic, amoeboid, coccoid, filamentous—and with diverse variants of amphiesma structure. The Phylogenetic relationships among peridinian algae remain largely unresolved today.

On the one hand, molecular phylogenetic studies have shown that the classical system does not reflect the actual Evolution of the order; on the other hand, they have only roughly outlined the main evolutionary lineages within Peridiniales. Some phenotypic traits correlating with genotypic distinctness in peridinians have been established. For instance, in peridinians, the amphiesma of the mother cell is not inherited by the daughter cells—during or after division, the amphiesma is shed, and the daughter cells completely synthesize a new amphiesma. In euhagamous species during sexual reproduction, typical copulation of gametes occurs, joining along their ventral sides to form a planozygote that remains in a motile state for a prolonged period (from several hours to several weeks). The overwhelming majority of peridinians have 40–80 chromosomes.

The characterization of the most important and interesting representatives is presented according to The complexity of cell coverings, types of morphological structure, and life cycle features, and does not carry phylogenetic significance.

The simplest structural plan is characteristic of the genus Gymnodinium. The alga is unicellular, monadic, and appears naked under an optical microscope, although it is actually covered by a soft amphiesma. It differs from related genera in that the transverse groove is located approximately in the equatorial zone of the cell.

All species of the genus are capable of heterotrophic nutrition via osmotrophic and phagotrophic pathways. In the latter case, the alga forms pseudopodia with a characteristic microtubular basket. A small number of species are obligate heterotrophs. However, the vast majority of species are mixotrophs possessing primary-type chloroplasts colored yellowish or brownish. Some representatives contain chloroplasts of other types. For example, in the blue-colored G. aeruginosum, the chloroplast arose As a result of endosymbiosis with a cryptophyte alga (fourth-type chloroplast). G. viride (=Lepidodinium viride) is green and possesses a second-type chloroplast, whose precursor was a green alga from the class Prasinophyceae.

Species of the genus inhabit predominantly marine plankton, with some species dwelling in fresh and brackish waters.

Molecular biological studies have shown that the genus is polyphyletic: some species originate from algae lacking a theca, while others lost the theca secondarily.

A special coenocytic structure is characteristic of Polykrikos cells. The alga is unicellular, more or less cylindrical, and contains two, four, or eight nuclei arranged one above the other. The transverse groove encircles the cell in a spiral 2–8 times. There is a single longitudinal groove running from the apical to the antapical poles. At the intersections of the grooves lie pairs of flagella—longitudinal and transverse. The number of pairs corresponds to the number of nuclei in the cell.

The alga is colorless and feeds osmotrophically and phagotrophically. An interesting feature of Polykrikos is the presence of specialized large ejectile structures—nematocysts—in the cytoplasm. Polykrikos inhabits coastal waters of subtropical and temperate seas.

The saltwater colorless alga Dinamoebidium is morphologically indistinguishable from a classic amoeba proteus: it moves and feeds using short pseudopodia and does not maintain a fixed shape. Under unfavorable conditions, the cell retracts its pseudopodia and becomes covered with a rigid wall, entering a cyst state. Upon completion of the resting period, the cyst protoplast divides to form 2–8 zoospores, which are morphologically similar to Gymnodinium cells.

Cells of the hemimonadic alga Hypnodinium retain longitudinal and transverse grooves and an eyespot, but lack flagella. An envelope (whose nature remains unclear) lies outside the amphiesma. The alga has several yellowish-brown chloroplasts and feeds photoautotrophically. Reproduction occurs via gymnodinium-like akinetic hemiozospores. The alga occurs in the plankton of coastal lagoons, particularly in the Black Sea region.

The coccoid alga Phytodinedria inhabits periphyton, settling mainly on freshwater filamentous green and blue-green algae. The alga's cells are hemispherical, covered by a wall, and contain numerous ribbon-shaped chloroplasts colored either brown or blue-green. Reproduction occurs via gymnodinium-like zoospores. Interestingly, the cells of the filamentous algae upon which Phytodinedria settles die off rapidly.

Another coccoid alga, Stylodinium, also colonizes freshwater filamentous algae (primarily of the genus Oedogonium) and destroys their cells. Unlike Phytodinedria, The Mechanism of Stylodinium's effect on the substrate is well studied and linked to the developmental biology of stylodinium.

The adult vegetative cell of Stylodinium attaches to the Oedogonium cell by a short stalk. At this stage, it is covered by a wall, lacks flagella, does not form pseudopodia, and feeds photoautotrophically. Upon completion of the growth phase, the wall ruptures, and an amoeboid covered with numerous axopodia emerges from the cell. The amoeboid settles on a healthy vegetative Oedogonium cell, retracts its axopodia, rounds up, and forms a single short pseudopodium. This pseudopodium destroys the wall of the victim cell, penetrates beneath the wall, and expands into a large pseudopodium with a characteristic microtubular basket. The pseudopodium engulfs the cytoplasm of the victim cell and draws it into its own cell, forming a large digestive vacuole. After digestion of the prey is complete, four gymnodinium-like zoospores are formed inside the amoeboid. The zoospores emerge, swim to new Oedogonium filaments, settle on them, and develop into a coccoid cell.

An example of a peridinian alga with a filamentous structural type is Dinothrix. The alga appears as unbranched filaments consisting of two to ten cells. The cells are covered by a layered, thick wall, are uninucleate, with numerous small yellow chloroplasts; sometimes a stigma persists in the cytoplasm. Another genus, Dinoclonium, resembles Dinothrix, but possesses distinctly branched filaments. Both algae reproduce by gymnodinium-like zoospores and are rare. Dinothrix was described from a marine aquarium, and Dinoclonium from a periphytic community of the French marine coast.

A significant portion of peridinians possess a well-developed theca. The most species-rich genera of this group are Peridinium and Dinophysis.

Peridinium cells resemble Gymnodinium in shape and protoplast organization, but are covered by a robust theca. The theca consists of two parts—an upper (epivalve) and a lower (hypovalve)—separated by a transverse groove. The epivalve is formed by fused apical, intercalary, and precingular plates, while the hypovalve is formed by postcingular and antapical amphiesma plates. In the zone where the plates meet, the theca forms coarse, prominent sutures. The epivalve and hypovalve are separated by a transverse groove running in the equatorial plane of the cell. The longitudinal groove is located on the hypovalve and only slightly extends onto the epivalve.

The overwhelming majority of species in the genus possess primary-type yellowish-brown chloroplasts. In some species (Peridinium balticum), the chloroplasts belong to the third type and arose as a result of endosymbiosis with a golden alga. A small number of species in the genus feed exclusively heterotrophically.

Species of the genus Peridinium inhabit mainly marine plankton, with only about 15% of species occurring in continental freshwaters.

Species of the genus Dinophysis are characterized by a transverse furrow displaced almost toward the apex and a strongly laterally compressed cell. The theca around the transverse furrow forms a funnel-shaped collar, while large wing-like outgrowths develop along the sides of the longitudinal furrow. Dinophysis species inhabit the marine plankton of cold, temperate, and subtropical zones.

Prorocentrales is the "youngest" order of dinophytes. The cells of prorocentrical algae differ significantly in appearance from the "typical" structural plan of dinophyte monad stages: the algae are covered by a sturdy theca, the main part of which consists of two Valves that fit together like walnut shells. An apical depression is located at the cell apex. The bottom of this depression is covered by several small plates, two of which are pierced by flagellar pores. Two heteromorphic and nearly isocont flagella emerge from the flagellar pores, directed forward. However, the ULTRASTRUCTURE OF THE flagella and their root system correspond to the typical structural plan of dinophytes. The cytoplasm contains a single dinokaryotic nucleus and yellowish-brown chloroplasts. Phagotrophic nutrition is not known in representatives of this order.

Cell division occurs longitudinally, with daughter cells—similarly to Goniaulacales—inheriting half of the theca from the mother cell and synthesizing the missing half.

The type genus is Prorocentrum, which unites over 100 species of marine planktonic algae. Some species cause toxic algal blooms in seas and coastal estuaries (in particular, Prorocentrum micans is a hazardous CAUSATIVE AGENT OF blooms in the Black Sea).

Distribution, Ecology, and Significance

Most dinophytes are marine planktonic organisms widely distributed in temperate, subtropical, and tropical zones. Developing in massive quantities in the seas, Dinophyta cause water blooms known as "red tides". For example, Protogoniaulax catenella causes red tides off the coast of British Columbia; Gymnodinium brevis, Protogoniaulax tamarensis, and P. excavata in the North Atlantic; and Prorocentrum minimum, along with certain Peridinium and Ceratium species, in the Pacific Ocean off the coasts of the USA and Japan. Since the mid-1980s, red tides caused by Prorocentrum micans have begun to appear annually in the Black Sea.

The Development of red tides is closely linked to the Life Cycle of the causative agents and depends on Temperature conditions, nutrient levels, and water salinity. The initiation of a red tide requires cysts to be transported from bottom sediments into surface water layers. This process can be facilitated by the mixing of surface and deep water masses during strong heating or cooling, or by the upwelling of saltier deep layers driven by meltwater at river mouths, etc. Once brought to the surface, the cysts germinate into monad cells. If the water is enriched with nutrients, the algae reproduce intensively, forming bloom patches that are driven toward the coast by tides, wind, or currents. The decline of a red tide is accompanied by the mass formation of planozygotes and cysts, which settle to the bottom. In the past, red tides occurred sporadically and only became widespread starting In the second half of the 20th century. It is believed that the primary factor making red tides a planetary phenomenon today is global ocean pollution.

Dinophyte water blooms are extremely dangerous. During red tides, massive mortality of aquatic organisms is observed—partly due to asphyxiation caused by the clogging of gill surfaces, and partly as a result of poisoning by dinophyte toxins.

The toxins of Dinophyta are neurotoxins, predominantly belonging to the saxitoxin group. To date, about fifteen neurotoxins have been identified in dinophytes, with saxitoxin (which acts similarly to curare poison) and tetrodotoxin being the most studied. In small quantities, these toxins cause respiratory tract irritation, Skin irritation, and allergic reactions in humans, while in large doses they lead to progressive paralysis, respiratory failure, and death.

The most common types of poisoning associated with Dinophyta are so-called "shellfish poisoning" and ciguatera. Shellfish poisoning results from consuming Mollusks such as Mytilus and Saxidomus, which accumulate algal toxins during red tides without being affected themselves. Ciguatera is caused by consuming the Internal Organs (primarily the Liver) of fish that have inhabited areas affected by dinophyte blooms.

In addition to red tides, Dinophyta can cause nocturnal bioluminescence of the sea (represented in the Black Sea by Noctiluca miliaris) and red water blooms in saline lakes (for instance, Glenodinium oculatum and Gymnodinium lens in Lake Saky).

In freshwater bodies, planktonic Dinophyta are rare (only a few species are relatively common, such as Peridinium polonicum, P. bipes, P. cinctum, and Ceratium hirundinella). Unlike planktonic forms, benthic and periphytic forms predominantly inhabit freshwater bodies.

Most dinophytes are thermophilic neutrophiles, although typical cryophiles (such as Gyrodinium pascheri, which vegetates in snow), acidophiles, and basiphiles also occur. Marine species prefer zones with a high organic matter content, whereas freshwater species are more frequently oligosaprobic.

The Position of Dinophyta in the System of the Organic World

The taxonomic position of dinophytes (dinoflagellates) within the eukaryote system has been debated not only by phycologists but also by protozoologists. Much like euglenophytes, dinoflagellates were once regarded as an order within the class Mastigophora. According to modern Protozoa classification systems, zoologists treat dinoflagellates as an independent class within the phylum Sarcomastigophora.

In botanical systems until the mid-1970s, dinophytes were also treated as a class and, based on similarities in coloration, starch presence, dorsoventral monad cells, and the absence of true cell walls, were grouped together with cryptophytes and raphidophytes into the division Pyrrophyta. However, data regarding cell ultrastructure—specifically concerning the pellicle, nuclear apparatus, chloroplasts, and flagella—led to the elevation of Dinophyta to the rank of an independent division.

In the 1980s, several researchers drew attention to certain similarities between the coverings of dinophytes and those of ciliates (Ciliata) and apicomplexans (Apicomplexa), notably their "alveolate" structure and the presence of a subpellicular microtubule layer. On this basis, a phylogenetic relationship between these three phyla was hypothesized, leading to the proposal to unite them into a distinct subkingdom or even kingdom, Alveolata. Molecular phylogenetic studies from the past decade have fully confirmed the validity of this hypothesis.

Dinophyta diverged as an independent division back among protistan ancestors, while acquiring their chloroplasts multiple times through symbioses with various algal groups.

Within Dinophyta, the predominant strategy remained a primitive plant-animal lifestyle—combining photosynthesis with the capacity for heterotrophic nutrition and active locomotion. Nevertheless, evolutionary attempts to transition toward a purely plant-like lifestyle also occurred, leading from unicellular attached forms to multicellular attached photoautotrophic plants.

¹ The morphological system structure is presented according to the variant outlined in the manual Freshwater Algae of the Ukrainian SSR (Topachevsky and Masyuk, 1984) and the monograph Algae: A Handbook (Wasser, Kondratieva, Masyuk et al., 1989).