The Position of Cyanobacteria in the World of Phototrophs
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Carlsberg Res. Commun. Vol. 42, p. 77-98, 1977 THE POSITION OF CYANOBACTERIA IN THE WORLD OF PHOTOTROPHS. by ROGER Y STANIER D~partementde Biochimieet G6n6tiqueMicrobienne 28, rue du Dr Roux, 75015 Paris, France EMIL CHR. nANSENlecture delivered at the Carlsberg Laboratory Centennial and the Inauguration of the Carlsberg Research Center on September 28th, 1976 Key words: prokaryotic photosynthetic apparatus; obligate photoautotrophy; oxidative and reductive pentose phosphate cycles; nitrogen fixation; oxygenic photosynthesis; facultative anoxygenic photosynthesis; cyanobacterial ecology; cyanobacterial developmental patterns Recent advances in our knowledge of the biological properties of the cyanobacteria (former ,blue-green algae,) are reviewed. The subjects discussed include: cyanobacterial cell structure and development; comparative as- pects of photosyntetic structure and function in prokaryotes; carbon metabolism and its relation to obligate photoautotrophy; and special properties of cyanobacteria that are of ecological significance (temperature rela- tionships, nitrogen fixation and facultative anoxygenicphotosynthesis). 1. INTRODUCTION seated functional differences between the two The largest evolutionary discontinuity among kinds of cells could be appreciated only after contemporary organisms lies at the cellular the molecular biological revolution. level; it permits us to distinguish two biological In addition to the organisms long recognized superkingdoms, eukaryotes and prokaryotes as bacteria, the superkingdom of prokaryotes (46, 43). The recognition of this fact is quite re- includes a large and widely distributed group of cent, since the differences between the phototrophic organisms, the cyanophytes or eukaryotic and the prokaryotic cell could not blue green algae. They can be defined as be rigorously formulated prior to 1960. A major microorganisms that harbor, within a typically technical advance, the application of electron prokaryotic cell, a photosynthetic apparatus microscopy to the study of biological fine struc- similar in structure and function to that located ture, was necessary to reveal the nature and ex- in the chloroplast of phototrophic eukaryotes. tent of the structural differences between pro- Their traditional classification as algae was, karyotic and eukaryotic cells; and the deep- accordingly, based on the resemblances be- R. Y. STANIER: Cyanobacteria Figure 1. Thin section of a unicellular cyanobacterium, Synechocystis ATCC 27178, in the course of division. 60,000 x. The cell membrane (CM) is surrounded by a wall composed of three layers: the peptidoglycan (Pg) layer, the outer membrane (Om) layer, both universal in cyanobacteria; and an additional structured (St) layer. The regularly spaced thylakoids (th) bear rows of phycobilisomes (pbs), attached to both surfaces. Cs, carboxysome; ri, 70S ribosome. 80 Carlsberg Res. Commun. Vol. 42, p. 77-98, 1977 R. Y. STANIER: Cyanobacteria tween the cyanophytan cell and one constituent with the dimensions and fine structure of a unit of the algal cell, its chloroplast. These orga- membrane, containing proteins and lipopoly- nisms are in reality bacteria, and I shall here- saccharides (16). These two wall layers, com- after refer to them collectively as cyanobacte- mon to all Gram negative bacteria, are accom- ria. panied in many cyanobacteria by additional The cyanobaeteria differ from the two other wall layers, an example of which is evident in groups of phototrophic prokaryotes, which figure 1. have always been classified among the bacteria The only form of cellular locomotion in cya- -namely, purple and green bacteria - in many nobacteria is gliding movement, widespread but respects: the mechanism of photosynthesis; the not universal. A layer of fibrils, intercalated be- fine structure and chemical composition of the tween the two layers of the Gram negative cell photosynthetic apparatus; nutritional require- wall, has recently been demonstrated in some ments and growth physiology. gliding cyanobacteria (24), and may possibly be Fifteen years ago, when we began to work on the organelle responsible for this type of move- cyanobacteria, these organisms were still con- ment. strued as algae, and their study was largely The cell membrane, usually of simple con- conducted, as it always had been, by phycolog- tour, is closely appressed to the peptidoglycan ists, with a heavy emphasis on descriptive wall layer. The most conspicuous internal struc- taxonomy and ecology. It was commonly be- tures of the cell are the regularly spaced photo- lieved that the isolation of pure cultures is ex- synthetic thylakoids, which occupy much of the ceptionally difficult, even though M. B. ALLEN cytoplasmic region, and bear attached to their (1) had made a promising start on this technical outer surfaces disc-shaped structures about 40 problem about 1950: indeed, most of the pure nm in diameter, known as phycobilisomes. The strains then in existence had been isolated by phycobilisome is a light-harvesting organelle, her. Accordingly, much of our initial work was and contains the cellular complement of phyco- directed to the isolation and purification of biliproteins, the major components of the cy- additional members of this group (47), an essen- anobacterial light-harvesting pigment antenna tial prerequisite for comparative experimental (21). The nucleoplasm has a typically prokary- studies. The news that these organisms are real- otic fine structure. The cytoplasm contains a ly bacteria has spread, thus encouraging other comparatively sparse population of 70S ribo- microbiologists to take up work on cyanobac- somes, a reflection of the low growth rates cha- teria. More significant information about their racteristic of most cyanobacteria. biological properties has emerged in the past Two classes of inclusions characteristic of cy- decade than in the preceding century. Some of anobacteria are carboxysomes and cyanophy- these recent advances will be reviewed here. cin granules. The former - polyhedral bodies bounded by a thin, non-unit membrane - occur in many other prokaryotes which use CO2 as 2. CELL STRUCTURE AND their major carbon source. They have been re- DEVELOPMENT cently isolated from a chemoautotroph, Thio- 2.1. Organization of the cyanobacterial cell. bacillus neapolitanus (38), and shown to be fil- Like the other photosynthetic prokaryotes, led with closely packed molecules of carboxy- cyanobacteria belong to the major sub-class of dismutase, the enzyme responsible for CO2 fixa- Gram negative bacteria, an assemblage now no tion in autotrophs. The carboxysome might be longer defined by the staining reaction of the considered the prokaryotic counterpart of the cell, but rather by the fine structure and mole- pyrenoid. cular composition of its wall. The cyanobacte- Cyanophycin granules (27) have been detect- rial cell wall contains at least two structurally ed only in cyanobacteria. The recent isolation distinct layers (fig. 1). The relatively thin and of these granules (39) has led to the interesting electron-dense innermost layer is composed of discovery that they are composed of a branched peptidoglycan (18). It is surrounded by a layer polypeptide which contains only two amino Carlsberg Res. Commun. Vol. 42, p. 77-98, 1977 81 R. Y. STANIER"Cyanobacteria Figure 2. Rod-shaped unicellular cyanobacteria of the genus Synechococcus. Phase contrast, 2000 x. A, ATCC 27194; B, ATCC 27145; C, ATCC 29534. acids: a polyaspartic acid core, bearing lateral cell division into a vegetative cell which can arginyl residues (40). This material accumulates attain a diameter of 20-30 ~tm, this development in the cell as cultures approach the stationary being accompanied by the formation and pro- phase, and probably serves as a nitrogen re- gressive thickening of a fibrous outer wall layer. serve. A rapid series of cell divisions unaccompanied by growth then takes place within the fibrous 2.2. Patterns of development wall layer, which breaks open to release as The simplest cyanobacteria are unicellular many as 1000 reproductive cells. In Dermo- rods or cocci, which reproduce by binary fission carpa, this process of multiple fission is the only (figs. 2 and 3). A few unicellular cyanobacteria mode of cell division. In other pleurocapsalean (fig. 4) reproduce by budding (51), a variant of cyanobacteria, exemplified by Pleurocapsa (fig. binary fission which also occurs in many other 6), enlargement of the reproductive cell is fol- bacterial groups (44). lowed by a series of binary fissions, to produce The pleurocapsalean cyanobacteria have a an aggregate of vegetative cells, held together remarkable developmental cycle, which is illu- by the contiguous fibrous outer wall layers; strated in figure 5 for one of the simplest repre- some (or all) of the vegetative cells then under- sentatives, Democarpa (52). A small reproduc- go multiple fission and release small reproduc- tive cell, 2-3 ttm in diameter, enlarges without tive cells. 82 Carlsberg Res. Commun. Vol. 42, p. 77-98, 1977 R. Y. STANIER:Cyanobacteria Figure 3. Coccoid unicellular cyanobacteria of the genera Gloeocapsa (A, B), the cells of which are enclosed by sheaths, and Synechocystis (C, D), the cells of which are not ensheathed. Phase contrast, 2000 x. A, ATCC 29159; B, ATCC 29113; C, ATCC 27171 ; D, ATCC 27819. Many cyanobacteria have a filamentous structure. The filament of cells, or trichome, elongates by intercalary divisions and repro- duces by breakage. In oscillatorian cyanobac- Figure 4. A unicellular budding