General Microbiology - Schlegel, H. 1987

Prokaryotes: A Systematic Review
Aerobic Oxygenic Phototrophic Bacteria (Cyanobacteria)

Due to their mode of reproduction via binary fission, cyanobacteria were long classified alongside Bacteria in the taxon Schizophyta. However, because of shared physiological traits, they were traditionally grouped with plants and referred to as blue-green Algae, and thus governed by the rules of botanical nomenclature. It was only after PROKARYOTES AND EUKARYOTES were clearly distinguished that this group of organisms was definitively assigned to the bacteria.

Cyanobacteria share with algae and higher plants The ability to perform oxygenic Photosynthesis, containing chlorophyll a and several other pigments common to the plant kingdom. This is why they were originally classified as blue-green algae. However, considering their mode of division, F. Cohn named them Schizophyceae and united them with Schizomycetes (bacteria) into the higher-order group Schizophyta. Indeed, based on cellular architecture, the presence of a murein Cell wall, 70S Ribosomes, and other defining markers, they must be classified as Gram-negative prokaryotes. Cyanobacteria represent the largest, most morphologically diverse, and most widespread group of photosynthetic prokaryotes. Thanks to their ability to thrive in extreme environments and fix molecular nitrogen, they play a vital ecological role in the complex web of nature.

Some cyanobacteria are motile. However, their locomotion never involves flagella, occurring solely through gliding across solid surfaces.

Morphology and systematics. Cyanobacteria encompass both unicellular and multicellular forms, which can be morphologically categorized into five distinct groups (Fig. 3.19).

Group 1: Chroococcalean cyanobacteria. These are unicellular rods and cocci. Cells exist either individually or as aggregates (colonies) held together by capsules or mucilage. Reproduction occurs exclusively through binary fission or budding. Representative genera include Synechococcus (formerly Anacystis nidulans), Gloeothece, and Gloeobacter violaceus.

Group 2: Pleurocapsalean cyanobacteria. These are also unicellular forms, distinguished by their ability to reproduce via multiple fission. During this process, numerous smaller cells, known as baeocytes, form within the dividing mother cell. Typical Examples include the genera Pleurocapsa, Dermocapsa, and Myxosarcina.

The following three groups are characterized by filamentous cell associations, forming trichomes—multicellular chains of cells. Growth occurs intercalary, through Cell Division within the trichome. Trichomes are capable of gliding motility. In many cases, reproduction involves the fragmentation of the trichome to form hormogonia. Consequently, these filamentous forms are sometimes referred to as hormogonian blue-green algae. Currently, three groups of trichome-forming cyanobacteria are recognized.

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Fig. 3.19. Schematic representations of selected cyanobacteria. Thick-walled cells with polar granules are heterocysts; dark cells are akinetes; thin lines outside the trichomes outline the sheaths. (Redrawn from Rippka R. et al., J. Gen. Microbiol., 111 [1979], 1.)

Group 3: Filamentous cyanobacteria lacking heterocysts. Trichomes consist exclusively of vegetative cells. Representative genera include Oscillatoria (the classic "oscillating alga"), Spirulina, Lyngbya, Phormidium, and Plectonema.

Group 4: Filamentous cyanobacteria possessing heterocysts. In trichomes growing under combined nitrogen-depleted conditions, cellular differentiation leads to The formation of heterocysts. Akinetes are also present in certain taxa. This group includes the genera Anabaena, Nostoc, and Calothrix.

Group 5: Filamentous cyanobacteria with heterocysts, which differ from the previous group by undergoing cell division in more than one plane. The best-known representative is the genus Fischerella.

Ecology. Cyanobacteria are widely distributed in lakes and other aquatic habitats, soils, and rice paddies. To the naked eye, they often appear as dark blue or black films on rocks, in the splash zones of freshwater lakes, and along marine littorals. The dark ("ink-like") streaks on limestone cliffs, typical of Water seepage areas, are formed by chroococcalean cyanobacteria. Eutrophic lakes frequently experience mass proliferation—or water blooms (Section 17.1.2)—of blue-green (Anabaena) or red (Oscillatoria rubescens) cyanobacteria. Due to their nitrogen-fixing capabilities, many cyanobacterial forms act as pioneer organisms in nutrient-deficient environments, such as marine sands or desert rocks, where they find shelter and moisture within narrow crevices. They are also highly resilient to other extreme conditions. Certain unicellular cyanobacteria (Synechococcus lividus) are so acid-tolerant and thermophilic that they thrive in acidic hot springs (pH 4.0, 70°C). Other species grow as symbionts: Nostoc as a partner in the lichen Peltigera, as well as within the roots of Cycas and Gunnera; and Anabaena azollae within leaf cavities of the tropical aquatic fern Azolla.

The Cell: Structure and subcellular components. In terms of ultrastructure, cyanobacteria closely resemble Gram-negative bacteria (Fig. 2.4). The protoplast is enclosed by a cell wall featuring an outer membrane and a lipopolysaccharide layer overlying the peptidoglycan layer. Many taxa secrete exopolysaccharides, which either dissolve into the surrounding medium as mucilage or form distinct capsules around individual cells and sheaths around trichomes.

The photosynthetic apparatus consists of thylakoids, which either run parallel to The Plasma Membrane or are extensively convoluted and located in the peripheral Regions of the Cytoplasm (Fig. 3.20). The thylakoid membrane contains chlorophyll a, β-carotene, and oxocarotenoids such as myxoxanthophyll, echinenone, and zeaxanthin, along with Components of the photosynthetic Electron Transport Chain. A hallmark feature of cyanobacteria (and red algae) is the presence of phycobilisomes—disc-shaped Protein Complexes attached to the outer surface of the thylakoids. They are composed of phycobiliproteins, most notably phycocyanin (75%), allophycocyanin (12%), and phycoerythrin, supplemented by colorless Polypeptides, which together account for 12% of their composition. Phycobiliproteins themselves consist of a protein moiety and prosthetic groups—phycocyanobilin or phyroerythrobilin. Functionally, these serve as light-harvesting pigments in cyanobacteria, transferring absorbed light energy predominantly to Photosystem II. Chlorophyll a supplies energy exclusively to Photosystem I. Phycobilisomes can comprise up to half of the total cellular protein.

Phycobilins share striking structural similarities with Bile pigments. Their synthesis begins with the formation of porphyrin; upon ring Cleavage, the carbon atom from the methine bridge is released as CO. The Biosynthesis of phycobilins is one of the few known biological processes that generates carbon monoxide.

Fig. 3.20. Photosynthetic membrane systems in cyanobacterial cells. A. Rows of phycobilisomes on the thylakoid membranes of Microcoleus vaginatus. (Wildman R.B., Bowen C.C., J. Bacteriol., 117 [1974], 866.) B. In Nostoc muscorum, double lamellae (thylakoid membranes) form undulating arrays, either singly or in groups. The outer boundary of the multilayered cell wall is visible. (Menke W., Z. Naturforsch., 16b [1961], 543.)

Among cyanobacteria, only Gloeobacter violaceus lacks thylakoids and phycobilisomes; its chlorophyll a is integrated into the plasma membrane, while phycobiliproteins form a continuous layer directly adjacent to the inner surface of the membrane.

In many cyanobacteria, The ratio of blue to red pigments is regulated by the light spectral composition. Exposure to green and blue light preferentially induces phycoerythrin synthesis, whereas red light promotes phycocyanin production. This complementary chromatic adaptation enables efficient light capture across diverse ecological niches (such as beneath a plant canopy or in deep, blue-shifted aquatic environments).

Cellular inclusions. Presumably, all cyanobacteria can store Polysaccharides (in the form of Glycogen granules) and polyphosphate granules. Poly-β-hydroxybutyric acid is accumulated by only a few species.

A reserve material unique to cyanobacteria is cyanophycin granules. Because they bind protein stains, their polypeptide nature is readily apparent. In this polypeptide—composed of aspartic acid residues—all free carboxyl groups are linked to Arginine; thus, the cyanophycin molecule consists of aspartate and arginine in a 1:1 ratio. This polymer Functions primarily as a nitrogen reserve: its concentration drops under nitrogen limitation and increases rapidly when a nitrogen source is reintroduced into the medium. Cyanophycin accumulates predominantly in heterocysts. It may also serve as a minor energy reserve, as arginine can be degraded under anaerobic conditions to yield Ornithine and carbamoyl phosphate, ultimately driving ATP regeneration.

Carboxysomes (see the end of Section 2.2.6) are highly prevalent in cyanobacteria. Planktonic cyanobacteria inhabiting stratified lakes, as well as bloom-forming species, almost universally possess gas vacuoles.

Specialized cells. Cyanobacteria possess highly differentiated cells that have no analogues in any other bacterial group. Let us examine these specialized cell types. Under light Microscopy, heterocysts immediately stand out due to their thickened cell walls, pale pigmentation, and strongly refractive polar granules. Transmission Electron microscopy has enabled a detailed analysis of their ultrastructure (Fig. 3.21). The polar granules were identified as cyanophycin granules, while the dense layers overlying the Gram-negative cell wall consist of polysaccharides in which glucose, galactose, mannose, and xylose are interconnected via β-1,3-glycosidic linkages. Heterocysts exhibit resistance to Lysozyme Digestion. They are connected to adjacent vegetative cells in the trichome by microscopic pores resembling plasmodesmata. Functionally, heterocysts serve as sites for nitrogen (N₂) fixation under aerobic conditions. They differentiate in filamentous cyanobacteria when combined nitrogen (NH⁺₄, NO^-₃) is scarce. This morphological differentiation is accompanied by significant biochemical shifts. Heterocysts synthesize Nitrogenase while breaking down phycobiliproteins, though chlorophyll a is retained. Consequently, mature heterocysts lack both phycobiliproteins and a functional photosystem II, rendering them incapable of O₂ evolution. They retain only photosystem I, enabling cyclic Photophosphorylation and ATP regeneration. Thus, heterocysts provide an optimal, oxygen-protected microenvironment essential for nitrogenase activity. Carbon compounds are supplied to them by neighboring vegetative cells, while fixed nitrogen is exported from heterocysts primarily in the form of glutamine.

Fig. 3.21. Schematic Cytology/practical/54.html">Longitudinal section of cyanobacterial cells. A. Vegetative cell. B. Heterocyst. 1 - plasma membrane; 2 - carboxysome; 3 - cyanophycin granules; 4 - fibrous layer; 5 - homogeneous layer; 6 - lamellar layer; 7 - polyphosphate; 8 - phycobilisome; 9 - ribosomes; 10 - thylakoid; 11 - vegetative cell; 12 - cell wall. (Stanier R. Y., Cohen-Bazire G., Ann. Rev. Microbiol., 31 [1977], 225; redrawn.)

Akinetes are resting cells characterized by their large size, heavy pigmentation, and thick cell wall. Like heterocysts, they are morphologically differentiated cells that can be located in the middle of a trichome (in Anabaena) or at its end (in Cylindrospermum), either within or On the surface (Fig. 3.19).

Hormogonia are short segments formed by the fragmentation of long trichomes, serving as Organs of reproduction. During hormogonium formation, oscillatorian cyanobacteria must sacrifice at least one cell of the trichome, as the cells are connected by a common peptidoglycan layer that cannot be ruptured at the cell junctions. This process is referred to as trancellular breakage.

Baeocytes ("small cells") are the reproductive cells of pleurocapsalean cyanobacteria. They are formed through multiple binary fission of a mother cell—a very large cell with a thick, fibrous exopolysaccharide envelope. A typical example is Dermocarpa, in which rapid, successive binary fissions yield anywhere from 4 to 1,000 baeocytes from a single mother cell.

Gliding motility. Many cyanobacteria are motile, including trichome-forming species, all hormogonia, and numerous baeocytes. They can move exclusively by gliding, a process that requires a solid substrate. This movement is accompanied by the Rotation of the trichome around its longitudinal axis, giving the filaments an oscillating appearance (hence the name Oscillatoria). For instance, in Oscillatoria princeps, a point marked on the trichome surface with India ink describes a helical path with a pitch angle of 60° during forward progression. Fine-structural Analysis of the cell wall has revealed fibrils oriented at this exact angle, suggesting that movement is driven by torsional waves generated by the fibrils. The direction of movement can be reversed. Many cyanobacteria are capable of phototaxis, concentrating in areas with optimal illumination.

Nitrogen Fixation. All heterocystous cyanobacteria are capable of fixing N₂. Heterocysts are cells morphologically and physiologically specialized for nitrogen fixation (see above). Surprisingly, it was discovered that the Genetic information (nif genes) required for nitrogenase synthesis is also present in pleurocapsalean cyanobacteria, despite the absence of filamentous, heterocyst-forming forms among them (the Oscillatoria group). Under normal growth conditions in the light, however, N₂ fixation does not occur because The Nitrogenase Enzyme is extremely sensitive to oxygen. Nevertheless, researchers succeeded in inducing nitrogenase synthesis and detecting the enzyme by employing a special technique: when cells are incubated in the absence of combined nitrogen under anaerobic conditions in the light, and the function of photosystem II is inhibited by adding dichlorophenyl-dimethylurea (thereby halting O₂ evolution), nitrogenase is synthesized. This approach demonstrated that more than half of the studied strains are capable of producing nitrogenase.

Among unicellular chroococcoid cyanobacteria, certain strains are also capable of fixing N₂. How these bacteria protect nitrogenase from photosynthetic oxygen remains unknown.

Anaerobic METABOLISM. Many cyanobacteria inhabit water layers containing high concentrations (approximately 5 mmol/L) of hydrogen sulfide. Studies on Oscillatoria limnetica have shown that in the presence of hydrogen sulfide, photosystem II is switched off, and an alternative, oxygen-free (anoxygenic) photosynthesis takes place According to the scheme

a process well known in anaerobic purple sulfur bacteria. However, the ability of many cyanobacteria to survive under anaerobic conditions likely plays a significant ecological role in only a few specific habitats.

Obligate photoautotrophy. Apparently, many cyanobacteria are obligate photoautotrophs, meaning they can grow only in the light. Only a few strains are capable of existing as chemoorganotrophs by oxidizing sugars in the dark. Under such conditions, their growth rate is invariably much lower than during photoautotrophic growth.

Prochloron. A novel photosynthetic Organism combining features of both prokaryotes and green algae was recently discovered. On the one hand, it possesses a typical Introduction/4.html">Prokaryotic Cell STRUCTURE (a Gram-negative cell wall containing peptidoglycan, lacking Organelles and a true nucleus, with a Genome Size of 3.6×10⁹ Da); on the other hand, along with chlorophyll $a$, it contains chlorophyll $b$, which is otherwise characteristic only of green algae and higher plants. It also differs from cyanobacteria by the absence of phycobiliproteins, cyanophycin, and poly-β-hydroxybutyric acid. This transitional form has been named Prochloron and is classified within an independent group of prochlorophytes. Prochloron grows as an ectosymbiont on various ascidians¹.

¹ Reports have recently emerged regarding the ISOLATION OF A free-living phototrophic bacterium containing both chlorophylls $a$ and $b$. - Ed. note.