Algology - Kostikov I.Yu. - 2009-2013

Chapter 20. Haptophyte Algae – Haptophyta

Haptophytes can be considered "living witnesses" of the era when the divergence of tubulicristates and platycristates began. Today, the division comprises about 500 species belonging to 80 genera. The vast majority of haptophytes are marine unicellular organisms.

Class="center">Taxonomic CHARACTERISTICS OF THE Division

Pigments and Reserve Nutrients

The METABOLISM/14.html">Chloroplasts of Prymnesiophytes are typically yellow or brown in color. This coloration is determined by the presence of chlorophylls a and c, which are masked by yellow xanthophylls: fucoxanthin and its derivatives—hexanoyloxy- or butanoyloxyfucoxanthin—along with diadinoxanthin and diatoxanthin. Among carotenes, only P-carotene has been detected.

The primary assimilation product is chrysolaminarin, which is deposited outside the Plastids. In haptophytes of the order Pavlovales, paramylon has also been discovered, which was previously considered a specific assimilation product exclusive to euglenophyte Algae.

Cytological Characteristics

From a cytological standpoint, the division is of particular interest because it demonstrates a wide array of Endoplasmic reticulum modifications associated with almost all major Organelles: The Nucleus, chloroplast, Cell coverings, Golgi apparatus, a specialized Structure known as the haptonema, partially the flagellar apparatus, and The process of mitosis.

Cell Coverings. The Cells are covered by a Plasmalemma, On the surface of which lie one or several layers of submicroscopic cellulosic scales or granules. On the cytoplasmic side, a large, encompassing cistern of The endoplasmic reticulum forms two additional inner layers of covering membranes (Fig. 20.1). Scales and granules are attached to each other and to the plasmalemma via acidic Polysaccharides. In some species, the scales become calcified, forming organomineral covering elements known as coccoliths. Scale Morphology serves as an important taxonomic feature, primarily at the species level (Fig. 20.2).

Fig. 20.1. Diagram of The structure of haptophyte cell coverings: 1, 2 - surface scales, 3 - plasmalemma, 4 - encompassing cistern of the endoplasmic reticulum, 5 - Golgi vesicle transporting a new scale to the surface.

Fig. 20.2. Scales of various species of the genus Chrysochromulina (after Esperland, Throndsen, 1986; Birkhead, Pienaar, 1995; Eikrem, 1996).

Nuclear Apparatus. The nucleus has a typical eukaryotic structure, yet with numerous specific features. For instance, the outer nuclear membrane directly transitions into the outer chloroplast membrane (Fig. 20.3). Furthermore, it forms invaginations that bear cytoplasmic Ribosomes. A clearly defined nucleolus is typically absent in haptophytes. Individual Chromosomes cannot be distinguished during metaphase; instead, all Chromatin condenses into a single dense chromatin plate. Kinetochores have not been found. Centrioles are also lacking, and the function of the spindle microtubule-organizing center is performed by a system of Golgi vesicles or (in algae of the order Pavlovales) electron-dense structures located at the tip of the microfibrillar ROOT of the longer flagellum.

Fig. 20.3. Diagram of the Cell Structure of haptophyte algae: 1 - surface scales, 2 - plasmalemma, 3 - peripheral encompassing cistern of the endoplasmic reticulum, 4 - flagellum, 5 - transition zone of the flagellum, 6 - basal body, 7 - haptonema, 8 - outer membrane of the chloroplast envelope (chloroplast endoplasmic reticulum), 9 - inner membranes of the chloroplast envelope, 10 - trithylakoid lamella, 11 - pyrenoid, 12 - thylakoid penetrating the pyrenoid, 13 - nucleus, 14 - outer membrane of the nuclear envelope continuous with the outer chloroplast membrane, 15 - mitochondrion with tubular cristae, 16 - invaginations of the outer nuclear envelope membrane (nuclear endoplasmic reticulum), 17 - endoplasmic reticulum channel, 18 - cisternae of the Golgi apparatus, 19 - Golgi vesicle with a surface scale, 20 - conventional Golgi vesicles, 21 - muciferous bodies, 22 - chrysolaminarin, 23 - polyphosphate body, 24 - vacuole, 25 - periplastidial space (summarized from microphotographs by Green, Hibberd, Pienaar, 1982; Birkhead, Pienaar, 1995, Eikrem, 1996).

Haptophytes exhibit open, semi-closed, or closed mitosis. Its distinctive feature is that during metaphase, chromosomes condense into a single massive plate pierced by channels, through which bundles of spindle microtubules pass. Two Golgi complexes abut the spindle, completely separating it from the flagellar basal bodies. In telophase, a new nuclear envelope forms from the cisternae of the Golgi apparatus and polar vesicles, while cytokinesis occurs via a Cleavage furrow formed by the plasmalemma.

Analyses of nucleotide sequence similarities across a range of nuclear genes have shown that the nuclear genome of haptophytes is, on the one hand, close to the nuclear genomes of cryptophytes, green, red, and glaucocystophyte algae, while on the other hand, it shares certain affinities with the genomes of plasmodiophorid slime Molds and centrohelid heliozoans.

Photosynthetic Apparatus. The chloroplasts of haptophytes are bounded by four membranes: the two outer ones form the chloroplast endoplasmic reticulum, and the two inner ones constitute the chloroplast envelope proper. The outer membrane directly continues into the outer nuclear membrane. Between the inner and outer membranes lies the periplastidial space containing its own 80S ribosomes.

Thylakoids in the chloroplast stroma are grouped in threes; an encompassing lamella is absent. A naked pyrenoid is quite frequently present. Chloroplast DNA consists of numerous fragments diffusely scattered throughout the chloroplast stroma.

An eyespot is found exclusively in algae of the order Pavlovales. It is located within the chloroplast, consists of a single layer of small globules directly adjacent to the chloroplast envelope, and is not coordinated with the flagella.

Thus, cytological features point to the secondary-symbiotic origin of haptophyte plastids. According to molecular phylogenetic reconstructions, the plastids of prymnesiophytes derive from red algae.

Mitochondria in haptophytes possess tubular cristae, similar to those of chromist algae and other stramenopiles. Studies of the Gene encoding the first subunit of mitochondrial cytochrome c have confirmed the hypothesis regarding the affinity of Haptophyta mitochondria with those of tubulicristates, specifically eustigmatophyte algae.

Another highly interesting finding is the presence of an animal-type Genetic Code derivative in the Mitochondrial DNA of haptophytes. For instance, whereas in higher plant mitochondria the UGA triplet Functions as a stop codon during Protein Biosynthesis, in Multicellular animals, Fungi, and red algae, this triplet codes for The amino acid Tryptophan. In haptophytes, UGA also codes for tryptophan and does not act as a stop codon.

Flagellar apparatus. Monad stages are represented by vegetative cells, zoospores, and Gametes. Motile cells bear two flagella of equal or unequal length, emerging from a subapical or lateral pit. The flagella are typically smooth; however, in algae of the order Pavlovales, both flagella possess simple (non-stramenopile) mastigonemes, with the longer flagellum also covered in submicroscopic granules.

Unlike the overwhelming majority of other algal phyla, the transition zone of the flagellum in haptophyte algae lacks a universal structure. Three MAIN TYPES OF transition zone structures are known in Haptophyta: a) an axosome, which is a large cap-shaped sleeve; b) a spiral structure; c) a system of intermediate rings. In some species, all these structures are present simultaneously (Fig. 20.4a), whereas in others, only two or just one of them can be found.

In addition to flagella, some haptophyte algae possess a unique flagellum-like non-motile organelle known as the haptonema. It is believed that the haptonema functions to attach cells to a substrate. Structurally, it is an outgrowth of the plasmalemma enclosing a single endoplasmic reticulum cisterna that wraps around 6–7 microtubules. The latter are a continuation of one of the flagellar roots (Fig. 20.4b).

In Haptophyta, with the exception of the genus Pavlova, the flagellar root system comprises three main microtubular roots (extending into the Cytoplasm from the basal bodies of the flagellas), one or two large additional (so-called crystal-like) roots connected to the main ones, and a single haptonemal root formed by the microtubules of the haptonema itself. The roots are interconnected and linked to the basal bodies via the contractile protein centrin (Fig. 20.4: c, d).

Fig. 20.4. STRUCTURE OF THE flagellum (a), haptonema (b), and The Root System of the flagellar apparatus (c - lateral view, d - top view) in haptophyte algae: 1 - basal body, 2 - axoneme, 3 - central microtubule doublet, 4 - peripheral microtubule doublet, 5 - spiral structure, 6 - axosome, 7 - intermediate rings, 8 - plasmalemma, 9 - peripheral endoplasmic reticulum cisterna, 10 - surface scales, 11 - endoplasmic reticulum cisterna within the haptonema, 12 - haptonemal microtubules, 13 - endoplasmic reticulum cisterna displaced to one side at the Base of the haptonema, 14, 15 - flagellar basal bodies (14 - left, 15 - right), 16 - 18 - main microtubular roots (16 - first, 17 - second, 18 - third), 19 - haptonemal root, 20 - accessory root of the second microtubular root, 21, 22 - microfibrillar roots of the first and third main roots, 23 - system of fibrillar connections between basal bodies (schematized after Beech, Wetherbee, 1988; Roberts, Mills, 1992; Gregson, Green, Leadbeater, 1993).

Other organelles. Typically, a single large Golgi complex is located between the flagellar basal bodies and the nucleus. Unlike in chromists, this complex is not pressed against the nuclear membrane. Alongside its routine functions, the Golgi complex participates in The formation of scales, which are subsequently transported outwards in vesicles and deposited onto The surface of the plasmalemma.

Muciferous bodies can quite frequently be observed at The Cell periphery, large chrysolaminarin droplets at its posterior end, and polyphosphate bodies and paramylon grains in pavlovalean algae as well.

Body Plans

The vast majority of haptophytes exhibit a monadal body plan. Coccoid forms are less common. Gametosporophytes of certain prymnesiales, isochrysidales, and coccolithales possess a filamentous type of structure. Under unfavorable conditions, most Haptophyta species are capable of shedding their flagella and transitioning into a palmelloid state.

Reproduction and Life Cycles

Haptophytes reproduce primarily through vegetative Cell Division into two. Reproduction via zoospores is observed only occasionally. An isogamous sexual process has been described in a small number of species.

In most species, The life cycle represents a cyclomorphosis. For instance, the Life Cycle of the marine alga Phaeocystis involves an alternation of monadal and coccoid stages. Furthermore, coccoid cells are capable of forming micro- or macroscopic mucous colonies, and upon The breakdown of these colonies, they can revert to the monadal state (Fig. 20.5a).

In eugamous species, the life cycle is rather complex, proceeding with a heteromorphic ALTERNATION OF GENERATIONS and sporic reduction, and is therefore haplo-diplontic.

For example, in the genus Pleurochrysis, the monadal vegetative diploid cells represent the sporophyte, formerly known as the "Hymenomonas" stage. They are covered with coccoliths and reproduce by binary fission or via zoospores. Under certain conditions, Meiosis occurs, resulting in the formation of four haploid zoospores that germinate into a haploid branched filamentous gametosporophyte previously described as an independent genus, "Apistonema". The gametosporophyte reproduces itself via zoospores or produces isogametes. Following copulation, the zygote, lacking a resting period, germinates into a monadal diploid coccolithophorid (Fig. 20.5b). The zoospores produced by the sporophyte possess a short, highly reduced haptonema, whereas in the zoospores of the gametosporophyte, the haptonema may be present or absent.

Fig. 20.5. Life cycles of haptophyte algae. a - cyclomorphosis (using Phaeocystis pouchetii as an example), b - haplo-diplontic life cycle with heteromorphic alternation of generations (using Pleurochrysis carterae as an example) (after Kornmann, 1955; Lee, 1980).

Taxonomic System of the Phylum

Based on the general cell plan, two clearly defined lineages can be traced within the phylum. The first Lineage unites all typical haptophytes, while the second comprises Representatives of the genus Pavlova. Essential differences between these lineages include The ability to accumulate paramylon, the presence of mastigonemes, submicroscopic scales on the flagella, an eyespot, THE POSITION OF the nucleus, and details of cytoskeletal architecture. In this regard, proposals have been made to divide the phylum into two classes or subclasses. However, molecular phylogenetic reconstructions based on both the nuclear and chloroplast genomes have not yet confirmed the validity of such a division. Therefore, today only a single class, Haptophyceae, is recognized within the phylum, which is divided into four orders: Isochrysidales, Coccolithales, Prymnesiales, and Pavlovales. The division into orders is based not only on the cell body plan, but also on the Structural Features of cell coverings and the presence of a haptonema (Table 20.1).

Table 20.1. Main Features of different orders of Haptophyceae

1. Prymnesiales. Comprises unicellular and colonial monadal and amoeboid isokont algae with a long or short haptonema. Coccoliths are absent; only microscopic cellulosic scales are present on the surface of the plasmalemma. Representatives of the order inhabit both marine plankton and inland freshwater bodies. Some prymnesiophyte algae are capable of causing toxic Water blooms. The most widespread are monadal algae, primarily species of the genera Chrysochromulina, Prymnesium, Corymbellus, and Phaeocystis. An example of an amoeboid prymnesiophyte is the genus Platychrysis (Figs. 20.5; 20.6).

2. Isochrysidales. Comprises unicellular and colonial monadal and coccoid algae that lack a haptonema and do not form coccoliths. The monadal cells of isochrysidaleans bear equal or slightly unequal flagella. They inhabit predominantly marine environments. A characteristic genus is Chrysotila (Fig. 20.6).

3. Coccolithales (Coccosphaerales, Coccolithophorales). Unites the so-called coccolithophorids—monadal or coccoid algae that lack a haptonema but possess calcified surface scales known as coccoliths. They are predominantly marine. Coccolithophorids flourished in the late Mesozoic, whereas in the Cenozoic the majority of species went extinct. Among extant genera, typical monadal representatives are Pleurochrysis and Hymenomonas (Figs. 20.5; 20.6), while the coccoid type of structure is characteristic of the genus Emiliania (Fig. 20.7).

4. Pavlovales. Comprises monadal algae with a distinct "pavlovalean" Cellular Organization. Specific features of the order include the presence of two flagella of unequal length (both with simple mastigonemes, and the longer one also bearing submicroscopic scales), an eyespot, paramylon, unique "pinecone-like" coccoliths, and a reduced haptonema. The nucleus occupies an apical position, and the microfibrillar flagellar root functions as a microtubule-organizing center (Fig. 20.7). They are distributed in the plankton of seas and estuaries. Currently, it includes only the genus Pavlova.

Fig. 20.6. Selected representatives of haptophytes: 1 - Chrysochromulina sp., 2 - Prymnesium parvum, 3 - Corymbellus aureus (a - single cell, b - colony), 4 - Platychrysis pigra (a - monad cell, b - amoeboid cell), 5 - Chrysotila lamellosa (a - solitary cells in palmelloid state, b - colony, c - zoospore), 6 - Hymenomonas roseola (adapted from Matvienko, 1965; Green, 1976; Billard, Gayral, 1972; Topachevsky, Masyuk, 1984).

Fig. 20.7. The coccolithophore Emiliania huxleyi (left) and cell structure diagram of Pavlova (right) (adapted from Klaveness, 1972, 1976; schematized after van der Veer, 1972, 1976).

Distribution, Ecology, and Significance

Haptophytes are predominantly marine algae and form a characteristic component of planktonic communities. Within the water Column, motile haptophyte cells undergo diurnal Migrations: by day, they concentrate in the warm surface layers of the euphotic zone at a depth of 30-80 cm, while at night they descend into colder, nutrient-rich deeper layers, occasionally reaching the thermocline (at depths up to 3-5 meters).

Gametosporophytes of certain coccolithophores (specifically, the filamentous "Apistonema" form of the genus Pleurochrysis) develop in the benthos or periphyton on the surface of calcified substrates, such as limestone, chalk cliffs, and mollusk shells.

Haptophytes (primarily members of Coccolithales) are particularly abundant in tropical and subtropical seas, where, together with dinoflagellates, they act as primary producers in the phytoplankton. Fewer Haptophyta are found in temperate and subpolar seas. Some species, such as Emiliania huxleyi, are cosmopolites.

Haptophytes can cause water blooms. For instance, Emiliania huxleyi and Phaeocystis pouchetii periodically trigger non-toxic blooms in the North Atlantic along the coast of Europe. It is now established that the mass proliferation of these species influences weather and climate. This impact is linked to the ability of Emiliania and Phaeocystis cells to release volatile dimethyl sulfide into the atmosphere during metabolism. Following photochemical transformation in the upper atmosphere, this compound forms moisture Condensation nuclei in clouds, leading to acid rain. Another agent of non-toxic blooms, the colonial alga Corymbellus aureus, regularly develops in massive numbers in the English Channel.

The first toxic prymnesiophyte bloom in marine environments was recorded in the late 1980s; it spanned the coastlines of Norway and Sweden, lasted for nearly two months, and caused mass mortality of farmed salmon in marine aquaculture and fish-rearing facilities. The bloom was caused by Chrysochromulina polylepis.

A dangerous agent of toxic blooms in brackish continental water bodies and estuaries is Prymnesium parvum. During mass development, it releases a mixture of proteophospholipids into the water known as ichthyotoxin. Once activated by sodium, magnesium, or Calcium Ions, the ichthyotoxin alters gill permeability and can cause mass fish kills. Outbreaks of Prymnesium blooms have been recorded in Bulgaria, Israel, Denmark, and the Netherlands.

Fossil Haptophytes

The earliest remains of haptophyte algae date back approximately 300 million years. However, "molecular clock" estimates derived from analyses of the nuclear gene encoding the 18S subunit of cytoplasmic ribosomal RNA indicate that the heterotrophic host cell of haptophytes arose about 850 million years ago. Autotrophic prymnesiophytes appeared later, 320-260 million years ago (based on chloroplast gene analyses encoding the large subunit of RUBISCO and the 16S subunit of chloroplast ribosomal RNA). According to the geological record, a rapid diversification of Haptophyta occurred during the Jurassic period (190-170 million years ago).

During the Cretaceous period, haptophytes became a dominant phytoplankton group in the World Ocean. Almost all chalk deposits from that era consist of the coccoliths of Coccolithales representatives. Interestingly, until the late 1970s, it was widely believed that chalk was composed of the skeletal remains and tests of foraminifera, testate amoebae, and radiolarians. Only the advent of scanning Electron Microscopy revealed the true origin of chalk.

At the end of the Cretaceous period, Haptophyta experienced a mass extinction. However, beginning in the mid-Tertiary period (55-40 million years ago), the phylum entered a new phase of biological progress, which continues to the present day.

Data on fossil haptophytes are widely applied in geological practice for dating sedimentary rocks and reconstructing planetary climates during the Mesozoic and Cenozoic eras.

The Position of Haptophyta in The system of the Organic World

The first haptophytes were described in the late 19th century. In the early 20th century, A. Pascher placed them among golden algae as separate genera within the class Chrysophyceae. In the 1960s, electron microscopy data revealed that prymnesiophytes possess several distinct features (notably a specialized flagellum-like structure, the haptonema); consequently, T. Christensen in 1962 separated them from Chrysophyceae into a new, distinct class, Haptophyceae. In 1976, D. Hibberd proposed the new name Prymnesiophyceae for these organisms to comply with the rules of the International Code of Botanical Nomenclature. During the 1980s, a large body of empirical evidence accumulated, not only confirming the distinct Separation of prymnesiophytes from golden algae, but also indicating their higher taxonomic rank. Therefore, in the late 1980s, haptophyte (prymnesiophyte) algae were elevated to an independent phylum, Haptophyta (Prymnesiophyta).

In the early 1990s, based on cytological data (primarily the presence of mitochondria with tubular cristae), haptophytes were regarded as a primitive side branch of Chromista, showing certain affinities with cryptomonads. Since the mid-1990s, numerous molecular phylogenetic reconstructions have indicated that Haptophyta constitute a unique transitional phylum positioned at the base of the kingdom Platycristates and subkingdom Plantae. Based on their nuclear genome, haptophytes resemble other platycristates, whereas their Mitochondrial Genome retains similarities to tubulocristates. Haptophytes acquired the capacity for Photosynthesis only after the divergence of platycristates and tubulocristates, resulting from a Symbiosis with red algae that subsequently transformed into the haptophyte chloroplast.