Phycology - Kostikov I.Y. - 2009-2013

Chapter 22. Glaucophytes – Glaucocystophyta

The phylum Glaucocystophyta includes about 10 species of free-living, microscopic unicellular Algae found in freshwater continental Water bodies. Fossil records of glaucophytes have not yet been discovered.

All known species of glaucophytes are photoautotrophs. The most fascinating and striking feature of this phylum is the presence of a unique photosynthetic apparatus represented by cyanelles—modified symbiotic blue-green algae that have lost The ability to exist independently outside the host Cell. Because of this, glaucophytes are often referred to today as "an example of symbiogenetic evolution in action." Research into plastid phylogeny at the molecular-biological level originally began with The Study of the genomes of both the host cell and the cyanelle.

In The Structure of other Organelles, glaucophytes share significant similarities with cryptophytes, green algae, and haptophytes.

Class="center">Taxonomic CHARACTERISTICS OF THE phylum

Pigments and reserve nutrients

The pigment composition of glaucophytes is practically identical to that of blue-green algae: chlorophyll a, β-carotene, and phycobilin pigments—phycocyanin and allophycocyanin—are present. Unlike Cyanophyta, phycoerythrin has not yet been reliably detected in representatives of Glaucocystophyta. Due to the high concentration of phycobilins, glaucophyte cyanelles have a blue-green color. Among xanthophylls, β-cryptoxanthin, which is also characteristic of cryptophytes, has been detected.

The assimilation product in Glaucocystophyta is ordinary starch. Unlike the starch of green algae and higher plants, glaucophyte starch is always deposited outside the photosynthetic apparatus.

Cytological characteristics

Although the cell coverings of glaucophytes are referred to as a pellicle, they more closely resemble the amphiesma of dinoflagellates: flattened membrane vesicles (lacunae), which may contain thin plates inside, are located beneath the Plasmalemma. From the cytoplasmic side, the lacunae are underlain by microtubules (Fig. 22.1). The presence of a microtubular layer distinguishes glaucophyte coverings from a typical amphiesma, while the presence of lacunae instead of protein strips differentiates them from the pellicle of euglenophytes.

Fig. 22.1. STRUCTURE OF THE pellicle in glaucophyte algae: 1 – plasmalemma, 2 – lacuna separated from the Cytoplasm by its own membrane, 3 – lacunar plate, 4 – underlying microtubules, 5 – flagellar ROOT microtubules (after Kies, 1989).

In some representatives (e.g., in the genus Cyanoptyche), a Cell wall is also observed on the outer side of the pellicle, formed by a layer of honeycomb-like subunits overlain by several layers of microfibrils of yet undetermined nature.

The nuclear apparatus is typically eukaryotic. The nuclear envelope consists of two membranes. A large nucleolus is located inside The Nucleus. Nuclear DNA is associated with histone Proteins and exhibits chromosomal Organization. An interesting feature of the glaucophyte nucleus is the presence of microfilament bundles within it. Aside from glaucophytes, similar nuclear microfilaments have been found in some red algae.

Analyses of individual genes (primarily the Gene encoding the 18S ribosomal RNA subunit) have revealed that the nuclear genome of glaucophytes is most closely related to the nuclear genomes of cryptophytes, red algae, and green algae, and is also quite close to The Genome of haptophyte algae.

Mitochondria in glaucophytes are branched, typically appearing in cross-sections as numerous small vesicles with lamellar cristae (Fig. 22.2), and can be considered a single mitochondrion. Cytological data, particularly the structure of the cristae, indicate that the mitochondrial system of glaucophytes is quite similar to the mitochondrions of other platycristates. Unfortunately, the Mitochondrial Genome of glaucophytes remains unexplored.

The photosynthetic apparatus of Glaucocystophyta is unique; it has no analogues among eukaryotic algae and consists of cyanelles. In literature, two viewpoints exist regarding The Nature of cyanelles: they are considered either precursors of true eukaryotic METABOLISM/14.html">Chloroplasts—symbiotic blue-green algae that have lost the ability to develop outside the host cell while retaining certain features of an independent Organism—or very primitive chloroplasts. A cell typically contains anywhere from two (genus Cyanophora) to many (genera Glaucocystis, Cyanoptyche) cyanelles (Fig. 22.2: a, b; 22.3).

Each cyanelle is delimited from the cytoplasm by a single cytoplasmic membrane. Beneath this membrane lies a thin, electron-dense layer composed of peptidoglycan (murein) (Fig. 22.2: c, d). Another membrane is located on the inner side of this layer. The presence of a murein layer between the outer and inner membranes clearly distinguishes the photosynthetic apparatus of glaucophytes from a typical chloroplast.

Fig. 22.2. Glaucophyte algae: a – general appearance of Cyanophora paradoxa under a Light Microscope; b – structural diagram of Glaucocystis; c, d – structure of cyanelles in Cyanophora paradoxa (c) and Cyanoptyche gloeocystis (d); e – phycobilisomes on thylakoid membranes; e–g – diagrams of the flagellar root system (e), flagellar surface (f), and mastigoneme Morphology (g) in glaucophytes. 1 – flagella, 2 – contractile vacuole, 3 – cyanelle, 4 – carboxysome, 5 – nucleus, 6 – nucleolus, 7 – starch granules, 8 – cell wall, 9 – Golgi apparatus, 10 – mitochondrion, 11 – oil droplet, 12 – Endoplasmic reticulum, 13 – vacuole with cell sap, 14 – outer membrane of the cyanelle, 15 – murein wall of the cyanelle, 16 – thylakoids, 17 – phycobilisomes, 18 – flagellar basal body, 19 – microtubular flagellar roots, 20 – multilayered structure, 21 – axoneme, 22 – mastigoneme (schematized after Kies, 1979, 1989; O'Kelly, 1992).

Inside the cyanelle, single thylakoids are arranged in concentric circles. The surface of the thylakoid membranes bears numerous phycobilisomes, similar to those of blue-green and red algae. In the central region of the cyanelle, one large or several small carboxysomes, formed by ribulose-1,5-bisphosphate carboxylase, are located. These carboxysomes are full analogues of the polyhedral bodies found in blue-green algae.

Cyanelles possess their own DNA, which is circular and not associated with Histones. Today, the cyanelle genome of one glaucophyte representative, Cyanophora paradoxa, has been fully sequenced; the genome of another glaucophyte, Glaucocystis nostochinearum, has also been studied in considerable detail. It has been established that the cyanelle genome contains approximately 10 times fewer NUCLEOTIDES than the genome of blue-green algae (about 125 kb instead of 1.2–1.5 Mb). Across almost all studied genes, cyanelles trace their direct Lineage to blue-green algae. However, it has also been established that cyanelles are "sister groups" rather than ancestors of the primary types of eukaryotic chloroplasts.

The flagellar apparatus. Monad stages of glaucophytes are heterokont and dorsiventral, and can be represented by either vegetative Cells (Cyanophora) or zoospores (Glaucocystis, Cyanoptyche). The flagella are heterokont and heterodynamic, emerging from a subapical depression that marks the beginning of a longitudinal groove. The shorter flagellum points forward and serves for propulsion. The longer flagellum lies within the longitudinal groove and acts as a rudder. A single contractile vacuole is located near the Base of the flagella. In zoospores, several dictyosomes are situated near the basal bodies; these participate (at least in Cyanoptyche) in constructing The Cell wall after cell movement ceases and it attaches to a substrate. Eyespots (stigmata) have not been detected in glaucophytes.

Each flagellum bears two rows of simple, non- tripartite mastigonemes, thus resembling the flagella of cryptophytes and certain green algae (Fig. 22.2: f, g).

The flagellar root system consists of four crosswise arranged microtubular roots and a multi-layered microtubular structure (Fig. 22.2: e). Each root comprises about 30 microtubules, and two of the four roots connect to the multi-layered structure. The outer sides of the multi-layered structure bear electron-dense layers, enclosing a layer of microtubules and a layer of parallel plates of unknown origin. The basal bodies themselves are interconnected by a fibrillar bridge.

Body Plans

Although only four genera of glaucophytes are known today, they represent Two Types of morphological structures: monadoid and hemimonadoid.

For instance, the genus Cyanophora is characterized by a monadoid structure type (Fig. 22.2, 22.3). The cells of Cyanophora are solitary and do not form colonies.

The genera Cyanoptyche and Glaucocystis exhibit a hemimonadoid structure. Each cell possesses a contractile vacuole, while heavily reduced flagella persist between the cell wall and the pellicle. These algae are united into gleocapsoid colonies consisting of 2–4–8 cells, resembling a system of nested mucilaginous vesicles. The differences between Cyanoptyche and Glaucocystis lie in the number and shape of cyanelles: in the former genus, cyanelles are small, numerous (up to several dozens), and do not form stellate clusters; in the latter, cyanelles are quite large, relatively few (8–15), and grouped into one or two star-shaped clusters (Fig. 22.3).

Fig. 22.3. Selected glaucophyte algae: 1 - Cyanophora paradoxa; 2 - Glaucocystis nostochinearum; 3 - Cyanoptyche gloeocystis. Contractile vacuoles are indicated by arrowheads (after Kies, 1989).

Reproduction and Life Cycles

Monadoid glaucophytes reproduce via vegetative Cell Division by binary fission in the motile state. Cell division is preceded by the division of cyanelles; thus, the Divisions of the cell and the cyanelles are well-coordinated.

Colonial representatives with a hemimonadoid structure (e.g., Glaucocystis) can reproduce by simple binary cell division, colonial fragmentation, and via zoospores. The morphology of glaucophyte zoospores is similar to that of vegetative Cyanophora cells.

Sexual reproduction has not been observed in glaucophytes, and their life cycle represents a cyclomorphosis.

Systematics of the Phylum

The phylum includes a single class, Glaucocystophyceae, and two orders, Cyanophorales and Glaucocystales. The first order unites species with a monadoid body structure and contains only one genus, Cyanophora. The second order comprises representatives with a hemimonadoid structure — the genera Glaucocystis, Cyanoptyche, and Gloeochaete (Fig. 22.3).

Distribution, Ecology, and Significance

All glaucophytes inhabit continental freshwaters. Species of the genus Cyanophora develop mainly in the plankton of ephemeral water bodies polluted with organic matter. Species of the genera Glaucocystis, Cyanoptyche, and Gloeochaete are periphytic inhabitants of floodplain water bodies. For instance, all three of these genera were once found in the same oxbow lake of the Danube River among the epiphytic growths on higher aquatic plants such as Hippuris vulgaris and Utricularia minor.

Glaucophytes are rare algae. Within the territory of Ukraine, two species from this phylum have been found: Cyanophora paradoxa and Glaucocystis nostochinearum.

Glaucocystophyta have no Practical Application in human activity. However, they are of paramount theoretical importance for resolving issues regarding the phylogeny of algae and the organic world as a whole.

Glaucophyte Cyanelles and THE ORIGIN OF Chloroplasts

Investigations of glaucophytes have played a major role in elucidating the ORIGIN AND EVOLUTION of the chloroplast. In this context, the historical development of views on the nature of cyanelles is quite interesting.

The first glaucophytes—the monadoid Cyanophora paradoxa and the hemimonadoid Cyanoptyche gloeocystis—were described at the beginning of the past century as representatives of different phyla: the first species was assigned to the class Cryptophyceae within the now-dismantled phylum Pyrrophyta, whereas the second species was placed in the order Tetrasporales of the phylum Chlorophyta. Both species were considered heterotrophs forming a stable Symbiosis with some organisms, likely blue-green algae. At that time, it was impossible to determine the deeper taxonomic position of the endosymbionts, so it was proposed to consider these "organisms" as blue-green algae of uncertain systematic position and to name them cyanelles.

In the 1970s and 1980s, the first monadoid and hemimonadoid glaucophytes were examined using Electron Microscopy. Based on the uniform structural plan of their flagellar stages and cyanelles, the glaucophyte species—previously placed in different phyla—were united in 1984 into a single class, Glaucocystophyceae, and subsequently segregated into a separate phylum, Glaucocystophyta (or Glaucophyta).

Electron microscopic studies from the 1970s to the early 1980s confirmed, on the one hand, that cyanelles are indeed structurally remarkably similar to blue-green algae. On the other hand, the results showed that, unlike Cyanophyta, cyanelles possess a reduced cell wall lacking the outer fibrillar Cellulose-pectin layer, although they retain a thin murein layer. These facts (obtained during the height of the controversy over the symbiotic origin of The Introduction/5.html">Eukaryotic Cell) sparked a debate regarding the nature of cyanelles: are cyanelles symbiotic blue-green algae, or do they represent a distinct, primitive type of plastid?

In the 1980s, the first attempts were made to answer this question using molecular biological studies of the cyanelle genome. As a result, two remarkably interesting features of glaucophytes were discovered: first, the size of the cyanelle genome (the number of nucleotide pairs in cyanelle DNA) is nearly identical to that of chloroplasts in other eukaryotes and is, on average, 10 times smaller than the genome of Cyanophyta. Second, two regions of so-called inverted nucleotide repeats were discovered in the cyanelle genome. These regions represented genes encoding chloroplast ribosomal RNA. Transcription of these fragments occurs in reverse directions (i.e., inverted). Inverted repeats encoding chloroplast ribosomal RNA have also been found in the chloroplast DNA of higher plants, yet they are absent in blue-green algae. In fact, molecular studies confirmed the hypothesis that cyanelles are chloroplasts rather than symbiotic blue-green algae. Furthermore, data on cyanelle Genome Size (specifically, its significant reduction compared to the prokaryotic genome) made it possible to understand why cyanelles cannot be cultured outside the host cell.

The recognition of cyanelles as a distinct, primitive type of plastid led to the Construction of a simple phylogenetic series explaining the origin of chloroplasts: a free-living blue-green alga enters into symbiosis with a heterotrophic host cell and, through genome reduction, transforms into a primitive plastid—the cyanelle. Subsequent reduction of the cyanelle, associated with the complete loss of its own cell wall, leads to The Emergence of a true chloroplast—the chloroplast of red algae. Red algae, via various pathways (in particular, through Darwinian evolution or secondary symbioses of the "heterotrophic eukaryote – red alga" type), give rise to all other algal phyla. Thus, glaucophytes appear as the most primitive eukaryotic plants. This viewpoint became very popular in the mid- to late 1990s; for example, it forms The basis of the material presented in the modern phycology textbook Algae. An introduction to phycology (C. Van den Hoek, D.G. Mann, H.M. Jahns, 1995, Cambridge Univ. Press).

Testing the hypothesis of glaucophyte primitiveness was carried out using molecular phylogeny Methods. The primary target for analysis was chosen to be the gene encoding the 16S subunit of ribosomal RNA in Bacteria, blue-green algae, glaucophyte cyanelles, and chloroplasts of eukaryotic algae across virtually all phyla (other genes were later analyzed as well—more than ten in total). The results proved unexpected (Fig. 22.4).

Fig. 22.4. Scheme of Phylogenetic relationships among Different types of chloroplasts. 1 - primitive blue-green algae originating from photoautotrophic anoxygenic bacteria; 2 - all other blue-green algae; 3 - blue-green alga originating from primitive Cyanophyta and serving as the ancestor of chloroplasts (the hypothetical so-called proplastid); 4-6 - chloroplasts formed via symbiosis of the proplastid with heterotrophic eukaryotes (so-called primary-symbiotic Plastids: 4 - cyanelles of Glaucocystophyta, 5 - chloroplasts of green algae, 6 - chloroplasts of red algae); 7 - chloroplasts of higher plants (derivatives of green algal chloroplasts); 8-9 - secondary-symbiotic chloroplasts formed following the symbiosis of a green alga with various heterotrophic eukaryotes (8 - chloroplasts of Euglenophyta, 9 - chloroplasts of Chlorarachniophyta); 10-14 - secondary-symbiotic chloroplasts formed following the symbiosis of a red alga with various heterotrophic eukaryotes, and their derivatives (10 - chloroplasts of Prymnesiophyta, 11 - Cryptophyta, 12 - chromist algae, 13 - the vast majority of Dinoflagellata, 14 - secondarily reduced plastids of Apicomplexa).

It has been established that primitive blue-green algae, originating from photoautotrophic bacteria, gave rise to five to seven lineages. All these lineages, with a single exception, comprise modern blue-green algae (including prochlorophytes) and represent evolutionary dead ends. However, one lineage leads directly to eukaryotic chloroplasts. It is believed that within this lineage, there existed a blue-green alga capable of entering into symbiosis with various heterotrophic eukaryotes—the so-called proplastid. The proplastid subsequently gave rise to Three types of plastids referred to as primary-symbiotic: the cyanelles of glaucocystophytes, the chloroplasts of green algae (the so-called chlorophyte-type plastid), and the chloroplasts of red algae (the rhodophyte-type plastid). All Other types of chloroplasts are either more recent derivatives of these primary plastids (e.g., the chloroplasts of higher plants) or arose as a result of secondary symbioses between primary-plastid algae and various heterotrophic eukaryotes.

Thus, it was established that cyanelles do not represent an intermediate stage in the photosynthetic apparatus series "photoautotrophic prokaryotes – true chloroplasts," but rather constitute an evolutionary dead-end variant of primary-symbiotic plastids.

Today, glaucocystophytes have once again become a "focus of special attention" for systematists and phylogeneticists in light of a renewed debate: whether the three types of primary plastids arose from a single symbiotic event between a proplastid and a heterotrophic eukaryote, or whether three separate symbiotic events occurred with different host cells, correspondingly giving rise to three distinct phyla of primary-plastid eukaryotes. Evidence supporting the first hypothesis has recently begun to emerge, though a definitive Conclusion remains a long way off.

THE POSITION OF Glaucocystophyta within the System of the living world

Today, the taxonomic position of glaucocystophytes within The system of living organisms is defined quite clearly. Based on mitochondrial ultrastructure, glaucocystophytes are typical platycristates and are therefore closely related to cryptophytes, red and green algae, higher plants, as well as Multicellular animals and true Fungi.

Regarding their photosynthetic apparatus, glaucocystophytes are plants possessing primary-symbiotic plastids known as cyanelles. A cytological feature characteristic of the primary-symbiotic nature of Glaucocystophyta plastids is the presence of only two membranes in the chloroplast envelope, while their apomorphic trait is the presence of a murein layer between these membranes. The cyanelles of glaucocystophytes and the chloroplasts of green and red algae form a single clade derived from blue-green algae.

Based on their assimilation products, nucleocytoplasmic organelle systems, and flagellar apparatus (particularly the structure of mastigonemes and the multilayered structure), glaucocystophytes are most closely related to green algae, and to a lesser extent, to cryptophytes. The affinity of these phyla is also supported by studies of more than ten nuclear DNA-encoded genes.

This entire suite of traits indicates that glaucocystophytes and green algae share a common ancestor. Primary-heterotrophic cryptophytes or their precursors are the most plausible candidates for this ancestral role.