Ultrastructure of the Cell Wall and Cell Division of Unicellular Blue-green Algae
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1 JOURNAL OF BACTERIOLOGY, Sept. 1968, p Copyright 1968 American Soziety for Microbiology Vol. 96, No. 3 Printed in U.S.A. Ultrastructure of the Cell Wall and Cell Division of Unicellular Blue-green Algae MARY MENNES ALLEN' Departmenit of Bacteriology antd Immuniology anid the Electroni Microscope Laboratory, Untiversity of Californlia, Berkeley, Californiia Received for publication 4 May 1968 The fine structure of the cell wall and the process of cell division were examined in thin sections of two unicellular blue-green algae grown under defined conditions. Unilateral invagination of the photosynthetic lamellae is the first sign of cell division in the rod-shaped organism, Anacystis nidulans. Symmetrical invagination of the cytoplasmic membrane and inner wall layers follows. One wall layer, which appears to be the mucopolymer layer, is then differentially synthesized to form the septum; the outer wall layers are not involved in septum formation. Centripetal splitting of the inner layer separates the two daughter cells. A second division, in a plane parallel to the first, usually occurs before the first daughter cells are separated. In the coccoid organism, Gleocapsa alpicola, the features of cell division are broadly similar; however, unilateral invagination of the lamellae is not observed and the second division takes place in a plane perpendicular to the plane of the previous division. Surveys of the fine structure of many bluegreen algae have included observations on the cell wall (17, 19), and some information is available on the mode of cell division (6, 8, 10, 11). Division in Anacystis montana is initiated by a medial constriction of the cell followed by introversion of the cell wall (6). Echlin (8) likened the structure of the cell wall and the mechanism of cell division in blue-green algae to that of grampositive bacteria. Quantitative chemical analyses of isolated cell walls from a filamentous bluegreen alga (10) and from a unicellular blue-green alga (4) have shown them to contain a mucopolymer similar in composition to that of gramnegative bacteria. Cell division in gram-negative bacteria has been described in terms of the behavior of the cell wall and cytoplasmic membrane as seen with the electron microscope by Steed and Murray (23) for Escherichia coli, by Cohen-Bazire et al. (3) for Chlorobium, and by Poindexter and Cohen- Bazire (18) for Caulobacter and Asticcacaulis. Septum formation in these organisms involves the annular invagination of the cytoplasmic membrane and the concomitant synthesis of a thin cell wall septum consisting of the mucopeptide layer alone (16). Centripetal splitting of the mucopeptide layer and synthesis of the outer layers follow. 1 Present address: Department of Biological Sciences, Wellesley College, Wellesley, Mass Time-lapse photomicrographs of cell growth and division in two types of unicellular bluegreen algae (1) showed that the division patterns were similar to those found in bacteria: the rodshaped algae divided consecutively in parallel planes while the coccoid algae divided in two or three planes perpendicular to each other. Light microscope observations do not, however, give information on the behavior of the cell wall and cytoplasmic membrane in division; therefore, observations were made on the two types of algae using the electron microscope to study cell division at the level of fine structure. MATERIALS AND METHODS Biological methods. Pure cultures of rod-shaped Aniacystis niidulanis (originally received from M. B. Allen) and coccoid Gleorapsa alpicola (originally received from G. P. Fitzgerald) were grown logarithmically at 25 and 35 C with 1,000 foot candles (ft-c) under conditions previously described (2). The generation time of G. alpicola was 5 hr at 35 C with 1,000 ft-c of illumination. During logarithmic growth under these conditions, an optical density of 0.2 at 750 nm = 0.26 mg (dry weight) per ml = 2.4 X 107 cells per ml. Under the same conditions, the generation time of A. nidulanis was 4 hr and an optical density at 750 nm of 0.2 = 0.16 mg/ml (dry weight) = 1.6 X 108 cells per ml. Electron microscope examinationt. Cells were harvested by centrifugation and fixed with Ryter-Kellenberger osmium tetroxide (21) or gluteraldehydeosmium under conditions described previously (2). 842
2 VOL. 96, 1968 CELL DIVISION IN BLUE-GREEN ALGAE 843 After fixation, cells were stained with uranyl acetate, dehydrated in an acetone series, and embedded in Maraglas with polymerization at 60 C for 48 hr. Sections were obtained with a diamond knife on a Porter-Blum ultramicrotome and poststained with Millonig's lead hydroxide (15) on 300-mesh grids. Sections were examined with a Siemens Elmiskop I electron microscope operated at 80 kv. RESULTS A. nidulans. The various stages in cell division were best seen in cells grown at 25 C. Those grown at 35 C showed only the initial invagination of cell membrane, or a complete septum. The terminology of Jost (14) will be used to describe the morphology and division of the cells as seen with the electron microscope. Immediately adjacent to the cytoplasmic membrane is an electron-transparent layer (LI) which is covered by a thin electron-dense layer (LI,), an electrontransparent layer (LI,,), and a thin mediumdense layer with a wrinkled appearance of about the dimensions of a unit membrane (Liv) as seen in Fig. 1 and 5. On the outside of the cell envelope is an irregular electron-dense overlayer which is probably a thin sheath (Fig. 5). The first indication of the onset of cell division is an asymmetrical invagination of the photosynthetic lamellae into the cytoplasm at the center of the cell (Fig. 1). In many cells, there is elaboration of membrane immediately adjacent to the cytoplasmic membrane in the area of photosynthetic membrane invagination (Fig. 1 and 3). Very little constriction of the cell was observed in the early stages of cell division (Fig. 2). The ensuing septum formation is symmetrical and does not involve participation of all layers of the cell wall. The cytoplasmic membrane and wall layers LI and LI, invaginate into the cytoplasm, and there appeared to be differential synthesis of layer LI, (Fig. 3 and 4) to form a broad septum (Fig. 5), the outer layers not being involved in septum formation. When the septum forms as far as the photosynthetic membranes, the lamellae on the side opposite the initial lamellar invagination appeared to be pushed before the cytoplasmic membrane (Fig. 2). When septum formation is complete (Fig. 5), the photo- FIG. 1. Ultrastructure of A. nidulans showing early stages in cell division. Arrow indicates the asymmetric photosynthetic lamellae invagination into the cytoplasm before septum formation. The cytoplasmic membrane (cm) and the layers of the cell wall are shown (layers LI, LI,, LI,,, and LIV). A slight amount of sheath materiat (S) cani be seen. Several polyhedral bodies (pb) are also visible in the cytoplasm. Membranous elaboration (e) is seen next to the cytoplasmic membrane. Osmium fixation. All markers indicate 0.1,um. X 60,000.
3 844 ALLEN J. BACTERIOL. Pk R FIG. 2 and 3. Ultrastructure of A. nlidulan1s showi,ig stages inl cell divisio,i. Arrows inldicate wall layer LII which is synthesized differenttial/v for septum formation. Asymmetric intvaginlationt of the lamellae is seeii inl botht cells. Osmium fixationt. X 60,000. FIG. 2. Ontly a smwall amoun?t of conlstrictionl of the cell is observed eveit after septum formation hass begunt. Photosyntthetic lamellae ont one side of the cell have intvagintated almost across the enttire cell anld the septumt begints to separate the lamellae onl the inlvaginwatinlg side, i/ito the two fulture daughter cells. FIG. 3. Elaborationl of membranle (e) ntext to the cytoplasmic membrante inl the area of septum formationl. A secon1d cell divisionl has be<gunl before the daughlter cells of the previous divisioni are completely separated.
4 9- A... K. FIG Ultrastructure of A. nidulans showing later stages in cell division. Note thickness of cell layer LI, in the septum. Growing septum pushes the lamellae on the side opposite the initial invagination into the middle of the cytoplasm and divides them into the daughter cells. Osmium fixation. FIG. 4. Septum formation is symmetrical with invagination occurring equally from each side of the cell. X 60,000. FIG. 5. Septum formation is complete. Sheath material (S) is especially evident. X 104,000. FIG. 6. Centripetal splitting of layer LI,. X 48,000. FIG. 7. Outline ofthe entire cell wall is evident around the ends of the daughter cells; cells are held to3ether by sheath material (S). X 48,
5 846 ALLEN J. BACTERIOL. synthetic membranes appeared, in some cells, to be cut off on one side of the cell (Fig. 4 and 6); in other cells, the lamellae appeared continuous around the end of the cell (Fig. 3). The two daughter cells are separated from each other by the growth of wall layer LI, across the plane of division, but they are maintained within the common enclosing outer wall layers as a single structural unit. In most cases, before final separation of the two daughter cells was complete, the beginning of the next septum was seen in a plane parallel to the last division (Fig. 3). To complete cell separation, the outer layers of the cell wall constrict and the septum is split, forming two complete cell walls. After the cytoplasm is completely separated, in many instances there is still a slight attachment between the cells (Fig. 7), probably of sheath material. G. alpicola. The same layers lying outside the cytoplasmic membrane were seen in thin sections of whole cells of the coccoid strain, G. alpicola, (Fig. 8 and 14), as in the rod-shaped A. nidulans. When observed with the electron microscope, the initial stages of cell division in this strain were the same as in A. nidulans, except that the photosynthetic lamellae did not invaginate in front of the growing septum. Before any constriction of the cell was observed, the cytoplasmic membrane and wall layers LI and LI, invaginated into the cytoplasm (Fig. 8, 9, and 14) and there was differential synthesis of the LI, layer. In most cases, the cell wall appeared to be distended in this area in early stages of division, due to the synthesis of LI, material (Fig. 8 and 9). Again, the outer layers of the cell wall are not involved in septum formation. There is some medial constriction of the cell, but the septum forms completely to separate the daughter cells from one another (Fig. 12) before final separation of the two cells takes place. A second division, in a plane perpendicular to the plane of the last division, usually begins before the previously formed daughter cells separate from each other completely (Fig. 13). Figure 14 shows two cells almost totally separated, with the septum of the next division partially formed. In G. alpicola, also, sheath material frequently holds cells together after cell separation has taken place. In many cells, after final separation, a polar cell wall thickening was observed in which wall layer LI, was much wider than normal (Fig. 15). The photosynthetic lamellae in this strain do not invaginate in front of the growing septum as they do in A. nidulans, but rather the septum appears to divide the lamellae into two parts, one part for each of the daughter cells (Fig. 10). DISCUSSION In the two unicellular blue-green algae examined in the present study, septum formation involves an annular invagination of the cell membrane and cell wall layers LI and LI,. Differential synthesis and widening of layer LI, produce a wide septum which is then split by the constriction of the outer layers of the cell wall. The majority of cells of both the rod-shaped and the coccoid strains observed were "two cells about-to-become-four" (20), as is the case for rod-shaped bacteria. The two daughter cells of the dividing alga were already, in most instances, in stages of cellular division. Septum formation and cell division can, therefore, be described in the same terms as for gram-negative bacteria (3, 18, 23). As in these bacteria, daughter cells of the blue-green algae are physically separated from one another by the septum, but are still bound together by their common wall. A wide LI, layer is found in both algae investigated here; in the bacteria, usually a very thin layer of the inner wall grows across the plane of division (16). Initiation of cell division by medical constriction of the cell (6) was not normally observed in these strains of blue-green algae. The cells of A. nidulans appear only slightly constricted when the cytoplasmic membrane and wall layers LI and LI, have invaginated into the cell cytoplasm to form the septum. In G. alpicola, the large amount of wall layer LI,, which is formed in the early stages of division, causes the cell wall to be distended in the area near septum formation. Division is symmetrical in both strains, with cytoplasmic membrane and wall invagination occurring equally on both sides of the cell. In the case of bacteria, such as Chlorobium (3) and Simonsiella (16), and a blue-green algal symbiont (11), cell division can be asymmetrical; the inner layers of the cell boundary move across the cytoplasm preferentially from one side until much of the septum is formed. An interesting asymmetry of lamellar invagination before the developing septum is observed in A. nidulans, where unilateral invagination of the lamellae takes place on one side of the cell as the first noticeable sign of cell division. The lamellae on the other side of the cell invaginate as cell division progresses. In G. alpicola, no invagination of lamellae was observed; the growing septum appears to separate the lamellae directly into the two daughter cells. Pankratz and Bowen (17) and Jost (14) reported this kind of lamellar division in filamentous blue-green algae. Lamellar connection with the cytoplasmic membrane in A. nidulans has been described
6 FIG. 8 and 9. Ultrastructure ojfg. alpicola. invaginiation of the cytoplasmic membraiie (cm) and wall layers LI and LII i,,to the cytoplasm beginis cell division. Cell wall is distenided at the poilnt ofseptum Jbrmationi by the synithesis of wall layer LI, No conistrictioni of the cell is observed; there is no early ilnvaginiationi of the photosynithetic lamellae as was observed in A. niidalanis. X 72,000. FIG. 8. All cell wall layers (LI, LI, Lllr, anld LIy) anzd the sheath (s) are very evidenzt. Osmium fixation. FIG. 9. Typical cell of G. alpicola shows photosynithetic lamellae (1), polyphosphate graniules (P), ntucleoplasm (n1), a small polyhedrial body (pb), a/id betweent the lamellae, ribosomes (r) anid electronz tranisparelnt bodies (et). Glutaraldehyde-osmium fixationt. 847
7 848 ALLEN J. BACTERIOL. Em giii FIG Ultrastructure of cell divisiont in G. alpicola. Note width of cell wall layer Li Cell wall layers LII Liv, anid the sheath are niot inivolved in the septum formationt. Osmium fixationz. X 90,000. FIG. 10. Growintg septum divides the photosynthetic lamellae into the daughter cells. Arrow intdicates lamellae which are cut by the septum, thereby divided inito the two futuire dauighter cells. FIG Some oj the lamellae in this cell appear to be pushed ahead of the growinig septum. X 60,000. FIG. 12. Septum formation is complete. X 60,000.
8 VOL. 96, 1968 CELL DIVISION IN BLUE-GREEN ALGAE 849 (2). The membranous elaborations seen in many cases at the point of septum formation in A. nidulans are perhaps similar to those seen in the filamentous blue-green algae (17) and in bacteria (18, 23) during septum formation. Lamellar elaborations were also recently observed in divisional stages of the cyanelle of the alga Glaucocystis nostochinearum (12). None of these elaborations of membrane appears to be the same as the lamellasomes described by Echlin (7) in A. nidulans, which generally appear to be invaginations of the photosynthetic lamellae and to have the dimensions of a double membrane. The elaborations seen in the present study have the dimensions of a unit membrane (Fig. 3). Membranous elements with the dimensions of a double membrane have been observed in A. nidulans and in two other recently isolated strains of rod-shaped Anacystis (M. M. Allen, Ph.D. Thesis, Univ. of California, Berkeley, 1966) at the ends of the cells, but never near the area of septum formations. Neither of these kinds of membrane elaboration have been observed in coccoid G. alpicola. The fine-structure observations indicate that it is possible to consider the blue-green algal cell wall and division in terms of the bacterial model. Plantlike division is never observed (13). The results of chemical analyses of isolated cell walls of both procaryotic cell types (10, 22, 24) give strong arguments in support of the morphological evidence. The isolated cell walls of bluegreen algae (4, 5, 9, 10) contain a fraction that shows a remarkable similarity to the mucopolymer layer of gram-negative bacteria, the layer to which the cell wall owes its shape and mechanical strength (22). The most logical terminology to use in describing the ultra-structure of the cell wall of blue-green algae would be that of Frank et al. (10), who have carried out analyses to coordinate chemical structure of the cell wall with the fine structure of the filamentous Phormidium. They interpreted their results to mean that the electron-transparent cell wall layer adjacent to the cytoplasmic membrane was the mucopolymer layer and that the middle lamella of the cross wall was formed from the plastic layer through pores in the mucopolymer layer. This interpretation of the mucopolymer layer appears unlikely; it is probable that this electron-transparent layer, seen also in the two unicellular algae observed in FIG. 13. The beginning ofa second septum formation in G. alpicola in a plane perpendicular to the first, before complete separation of the first daughter cells. The cytoplasmic membrane (cm), cell wall layers Li, LI,, LI,,, and LIv and the sheath material (s) are evident. Osmium fixation. X 90,000.
9 FIG. 14. Daughter cells are connected to each other only by sheath material (S). All the layers of the cell surface are visible around the ends of the cells. A division in a plane perpendicular to the last division has begun. Osmium fixation. X 90,000. FIG. 15. Ultrastructure ofg. alpicola showing polar thickening ofthe cell (pt). Glutaraldehyde-osmium fixation. X 72,000. Reproduced by permission of Academic Press, Iic., New York (see Acknowledgments). 850
10 'VOL. 96, 1968 CELL DIVISION IN BLUE-GREEN ALGAE 851 this study as LI, is an artifact of preparation. The width varies from cell to cell or from region to region within the same cell, and many times the cell membrane is appressed directly to the LI, layer. From studies on gram-negative bacteria (3, 16, 18, 22), it appears that the mucopolymer layer is electron dense and lies next to the cytoplasmic membrane. It appears likely that the cell wall layer LI, is the mucopolymer layer in these blue-green algae as well, although simultaneous chemical and fine-structural analyses must be done on these two algae to confirm this assumption. Chemical analyses of the cell walls of A. nidulans by Drews and Meyer (4) showed the mucopolymer content to be 28% of the dry weight of isolated cell walls, so that a large part of the cell wall or septum should be mucopolymer. Jost (14), on the other hand, in freeze-etched material, found granules in different quantities on layers he interpreted to be mucopolymer and middle lamella (after Frank et al., 10), therefore implying that there are indeed two distinct layers in the cross walls of Oscillatoria. The only thickening of the cell wall (Fig. 15) which has been reported previously in blue-green algae was in the terminal cell of Symploca muscorum, where the end wall showed thickening (17). ACKNOWLEDGMENTS This investigation was supported by National Science Foundation grant GB-4112 to R. Y. Stanier and by a Public Health Service predoctoral fellowship (1-F1-GM-21,008-01) to M. M. Allen. I am indebted to Roger Stanier for the many helpful suggestions he offered during the preparation of this manuscript. I also thank James McAlear and his staff of the Electron Microscope Laboratory for the use of facilities, and particularly Paula Stetler for technical assistance. Figure 15 was first published in The Chlorophylls, p. 315 [L. P. Vernon and G. R. Seely (eds.), Academic Press, Inc., New York] and is used here by permission of the publisher. LITERATURE CITED 1. Allen, M. M., and R. Y. Stanier Growth and cell division of some unicellular blue-green algae. J. Gen. Microbiol. 51: Allen, M. M Photosynthetic membrane system in Anacystis nidulans. J. Bacteriol. 96: Cohen-Bazire, G., N. Pfennig, and R. Kunisawa The fine structure of green bacteria. J. Cell Biol. 22: Drews, G., and H. Meyer Untersuchungen zum chemischen Aufbau der Zellwande von Anacystis nidulans und Chlorogloea fritschii. Arch. Mikrobiol. 48: Drews, G., and W. Gollwitzer Untersuchungen an der Polysaccharidfraktion der Zellwande von Anacystis nidulans. Arch. Mikrobiol. 51: Echlin, P The fine structure of the bluegreen alga Anacystis montana f. minor grown in continuous illumination. Protoplasma 58: Echlin, P Intra-cytoplasmic membranous inclusions in the blue-green alga Anacystis nidulans. Arch. Mikrobiol. 49: Echlin, P., and I. Morris The relationship between blue-green algae and bacteria. Biol. Rev. 40: Frank, H., M. Lefort, and H. H. Martin Chemical analysis of a mucopolymer component in cell walls of the blue-green alga Phormidium uncinatum. Biochem. Biophys. Res. Commun. 7: Frank, H., M. Lefort, and H. H. Martin Elektronenoptische und chemische Untersuchungen an Zellwanden der Blaualgen Phormidium uniciniatum. Z. Naturforsch. 17b: Hall, W. T., and G. Claus. Ultrastructural studies on the blue-green algal symbiont in Cyanophora paradoxa Korschikoff. J. Cell. Biol. 19: Hall, W. T., and G. Claus Ultrastructural studies on the cyanelles of Glaucocystis nostochinearum itzigsohn. J. Phycol. 3: Jensen, W. A Specialization of the plant cell, p In D. Mazia and A. Tyler (ed.), General physiology of cell specialization. McGraw-Hill Book Co., New York. 14. Jost, M Die Ultrastruktur von Oscillatoria rubescens. Arch. Mikrobiol. 50: Millonig, G A modified procedure for lead staining of thin sections. J. Biophys. Biochem. Cytol. 11: Murray, R. G. E., P. Steed, and H. E. Elson The localization of the mucopeptide in sections of the cell wall of Escherichia coli and other gram negative bacteria. Can. J. Microbiol. 11 : Pankratz, H. S., and C. C. Bowen Cytology of blue-green algae. I. The cells of Symploca muscorum. Am. J. Botany 50: Poindexter, J. L. S., and G. Cohen-Bazire The fine structure of stalked bacteria belonging to the family Caulobacteraceae. J. Cell Biol. 23: Ris, H., and R. Singh Electron microscope studies on blue-green algae. J. Biophys. Biochem. Cytol. 9: Robinow, C. F Nuclear apparatus and cell structure of rod-shaped bacteria, p In R. J. Dubois (ed.), The bacterial cell. Harvard Univ. Press, Cambridge, Mass. 21. Ryter, A., and E. Kellenberger Etude au microscope electronique de plasmas contenant
11 852 ALLEN J. BACTERIOL. de l'acide desoxyribonucleique. I. Les nucleoides des bacteries en croissance active. Z. Naturforsch. 13b: Salton, M. R. J The bacterial cell wall. Elsevier Publishing Co., Amsterdam. 23. Steed, P., and R. G. E. Murray The cell wall and cell division of gram negative bacteria. Can. J. Microbiol. 12: Work, E., and D. L. Dewey The distribution of diaminopimelic acid among various microorganisms. J. Gen. Microbiol. 9.AQ4-409.
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