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Chapter 3 : Cyanobacterial Phylogeny and Development: Questions and Challenges

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Abstract:

This chapter provides a selective overview of present knowledge of cyanobacterial morphological forms and their development. Due to the paucity of physiological variation among cyanobacteria, their classification has relied heavily on their morphological complexity. Recent work has revealed the cyanobacterial cell wall to be more complex than once thought. The generation of an anaerobic interior in the heterocyst requires a series of major modifications to the original vegetative cell. Due to their highly differentiated nature, heterocysts are readily distinguished from vegetative cells, usually being larger, with thickened cell walls and less-granular cytoplasm. The developmental control of gene expression was cleverly demonstrated by Elhai and Wolk with the genes, which encode bacterial luciferase, as transcriptional reporters. Many o f the properties of akinetes are suited to their role in surviving environmental conditions adverse for vegetative growth. The major stimulus for akinete germination appears to be an increase in light intensity, usually achieved in the laboratory by diluting an akinete-containing culture with fresh or used medium. Hormogonia are short, undifferentiated filaments produced by fragmentation of the parent trichome and which often possess gliding motility. Although the most clearly differentiated cells are heterocysts and akinetes, there is increasing evidence for more subtle forms of differentiation in at least two genera, and . Cyanobacteria pose many unanswered questions, some of which have been discussed in the chapter.

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 1
FIGURE 1

Schematic diagram illustrating some of the possibilities for morphological development in filamentous cyanobacteria. When grown in the presence of a source of combined nitrogen, the filament consists entirely of undifferentiated vegetative cells (2). At the end of the exponential growth phase, when light (energy) becomes limiting, some vegetative cells can differentiate into the spore-like cells called akinetes (A), which, in the absence of heterocysts, are randomly placed within the filament (1). In the absence of combined nitrogen, the vegetative filament differentiates the highly specialized N2-fixing cells, heterocysts, at spaced intervals within the filament (H) and in terminal positions (TH). Heterocysts are characterized by their thickened cell walls, relatively agranular cytoplasm, and polar bodies at the point of attachment to vegetative cells (two in heterocysts within the filament but only one in terminal heterocysts) (4). During their development heterocysts pass through an intermediate stage, the proheterocyst (PH), which, unlike the mature cell, does not have the thickened cell wall and polar bodies and is able to dedifferentiate in the presence of combined nitrogen (3). When akinetes develop in N-fixing cultures, they do so at locations with a spatial relationship to the heterocysts (see the text for details), such as midway between them (5). Akinetes can germinate and give rise to filaments with or without heterocysts, depending on the availability of combined nitrogen. Hormogonia are short, motile filaments lacking heterocysts, which develop as a result of a variety of stimuli (see the text for details). Their formation usually involves the rapid, synchronized division of vegetative cells without concomitant growth, followed by fragmentation of the filament to release heterocysts and motile hormogonia. The latter can give rise to heterocystous or nonheterocystous filaments, depending on the availability of combined nitrogen. Hormogonia can also serve as the infective agents in the establishment of symbiotic associations with plants. ( )

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 6
FIGURE 6

Diagrammatic comparison of die developmental cycles of pleurocapsalean cyanobacteria. Stages A to F are defined in Table 1 . The small dotted circles represent baeocytes that are not surrounded by a fibrous outer wall layer at the time of release and are consequently motile. The small solid circles represent baeocytes that arc surrounded by a fibrous layer and are immotile. ( )

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 3
FIGURE 3

Schematic diagram of a thin section ofa cyanobacterial cell. C, carboxysome; CPG, cyanophycin granule; T, thylakoid; P, polyphosphate granule; N, nucleoplasm region; G, glycogen granules; PB, phycobilisome; GV, gas vesicle. Inset A is an enlarged view of a thylakoid, showing paired unit membranes. Inset B is an enlarged view of the cell envelope, showing the outer membrane, the peptidoglycan layer, and the cytoplasmic membrane. ( )

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 4
FIGURE 4

(A) Diagram of the cell wall of sp. The peptidoglycan layer (PG) is perforated by large pore pits (LP) up to 70 nm in diameter, which bring the cytoplasmic membrane (CM) close to the outer membrane (OM). The large pore pits are seen in cross-section in the lower half of the diagram and appear as circles when viewed from above in the top half of the diagram. Junctional pores (JP) traverse the peptidoglycan between cells and meet at the surface, appearing as a single row of small circles when viewed from above in the top half of the diagram. ( ) (B) Electron micrograph of a thin longitudinal section of an unidentified member of the order . The large pore pits (LP) can be seen as bright circles scattered throughout the peptidoglycan. The plane of the section is within the peptidoglycan layer, with the result that the junctional pores (JP) appear as parallel rows of small, closely positioned circles at the cell cross walls rather than the single rows that would be seen at the surface of the peptidoglycan. The sample was fixed in osmium tetroxide and stained with uranyl acetate. Bars, 0.2 µm. (Electron microscopy by Denise Ashworth.)

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 5
FIGURE 5

A fibrillar array in the cell wall of a motile cyanobacterium. (A, C, and D) Transmission electron micrographs of thin sections of sp. strain FT2 filaments. (A) Longitudinal section. At the top of the figure, beyond a cell septum, the section has grazed the surface of the filament, revealing an array of parallel fibrils running at an angle of approximately 25 to 30° to the filament long axis. Bar, 400 nm. (C) Part of a transverse section showing an end view of the fibrillar array in the cell wall. Bar, 200 nm. (D) Enlarged view of part of panel C, showing the double line of the outer membrane (om) covering the fibrillar array and dipping between each pair of fibril (s) (f) to contact the electron-dense peptidoglycan layer (pg). Bar, 50 nm. (B) Transmission electron micrograph of part of a filament of sp. strain FT3. An actively motile sample was crushed between glass slides and negatively stained. The micrograph shows several cells from which the contents have been extruded and whose walls have been flattened, bringing the fibrils at the front and back of the filament into close contact, allowing them to be viewed simultaneously. The fibrils run helically around the entire surface of the filament, producing the observed criss-cross effect because those in the wall in the foreground run in a different direction than those in the wall in the background. Bar, 500 nm. ( )

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 2
FIGURE 2

Photomicrographs illustrating some of the differentiated cell types of cyanobacteria. (A) sp. strain CA grown in the presence of nitrate, which completely suppresses heterocyst development. (B) sp. strain CA grown in the absence of combined nitrogen, showing the regular spacing of heterocysts, which are the sites of N fixation, and a developing proheterocyst (arrow). (C) , showing large, granular akinetes developing immediately adjacent to a heterocyst. The two akinetes below the heterocyst show a characteristic-gradient of maturity, with the largest and oldest closer to the heterocyst. (D) An old culture of nitrate-grown sp. strain CA in which all vegetative cells have transformed into spherical akinetes. Although the akinetes have become separated, as a result of pressure created by the coverslip being placed onto the sample, the line of the original filaments can still be seen. Dilution of such a culture leads to germination of the akinetes. If the medium used for dilution does not contain a source of fixed nitrogen, the short filaments which emerge from the akinete coats each contain a heterocyst (E). Bars, 10 µm. Panels C and D were made with phase-contrast optics. Panels A and B reproduced from with permission of the publisher (copyright CRC Press Inc.); panel C reproduced from with permission of the publisher; panels D and E reproduced from with permission of the publisher.

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 7
FIGURE 7

Development of individual baeocytes of sp. strain PCC 7302 (A), sp. strain PCC 7312 (B), and sp. strain PCC 7516 (C) on agar medium. The number in each photomicrograph indicates the elapsed time, in hours, after the initial observation. The baeocytes follow the developmental cycles shown diagrammatically in Fig. 6 , culminating in multiple fission and the production of more baeocytes. The magnification is the same for all photomicrographs. Bars, 10 µm. ( )

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 8
FIGURE 8

(A) Electron micrograph of a thin section of a cell of sp. strain PCC 7307 which has divided into numerous baeocytes, each of which is surrounded by a distinct fibrous layer. (B) Electron micrograph of a thin section of a cell of sp. strain PCC 7326. The two basal cells, which are surrounded by a clear fibrous layer, are the products of the previous binary fission, while the apical cell has undergone multiple fission to produce many baeocytes, which do not have a fibrous layer. Bars, 1 µm. ( )

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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Image of FIGURE 9
FIGURE 9

Electron micrographs of thin sections of sp. strain PCC 7304 grown in liquid medium. (A) Cell immediately prior to multiple fission, containing many separate nucleoids (N) frequently associated with carboxysomes (C). (B) Cell which has completed multiple fission and is filled with baeocytes, each of which is surrounded by a peptidoglycan layer and outer membrane but not by an F layer. Bars, 1 µm. ( )

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3
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References

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Tables

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TABLE 1

Comparison of the developmental cycles of pleurocapsalean cyanobacteria

Citation: Adams D. 2000. Cyanobacterial Phylogeny and Development: Questions and Challenges, p 51-81. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch3

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