Ultrastructure of Blue-Green Algae'
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1 JOURNAL OF BACTERIOLOGY, Mar. 1969, p Copyright 1969 American Society for Microbiology Vol. 97, No. 3 Printed in U.S.A. Ultrastructure of Blue-Green Algae' E. GANTT AND S. F. CONTI Radiation Biology Laboratory, Smithsonian Institution, Washington, D.C , and Microbiology Department, University of Kentucky, Lexington, Kentucky Received for publication 29 November 1968 Two freshwater blue-green algae, Tolypothrix tenuis and Fremyella diplosiphon, and an oscillatorialike marine alga, were found to possess structures on the photosynthetic lamellae which appear to correspond to the phycobilisomes of red algae. These homologous structures are important because they contain the phycobilins which are accessory pigments involved in photosynthesis. As in the red algae, the phycobilisomes were attached on the outer side of each lamellae, i.e., the side facing away from its own membrane pair. Although our study on Anacystis nidulans has not thus far revealed the presence of phycobilisomes, some observations were made on the structure of the polyhedral bodies. After negative staining, the polyhedral bodies were seen to be composed of regularly spaced subunits arranged in a crystalline array. Elongated segmented rods, which differed from the polyhedral bodies, were found in the nuclear region of apparently healthy Tolypothrix cells. Numerous studies on blue-green algae have elucidated various aspects of their fine structure [see Echlin and Morris (5) and Pankratz and Bowen (17) for extensive literature reviews]. It has generally been accepted that chlorophyll a is located in the photosynthetic lamellae. However, the location of the phycobiliproteins has largely been ignored by morphologists using electron microscopy. The role of the phycobiliproteins as accessory pigments and their involvement in energy transfer of photosynthesis (4, 6) lends special significance to their physical location. As has been shown (7-9) in the red alga Porphyridium cruentum, the phycobiliproteins are present as aggregates (phycobilisomes) on the photosynthetic lamellae. Because of our interest in the localization of phycobiliproteins, we deemed it necessary to examine various bluegreen algae for the presence of phycobilisomes. Our success in finding them was mediated by difficulty in obtaining consistent preservation with known fixation procedures. It was difficult to obtain the same excellent fixation which is necessary for the preservation of phycobilisomes in red algae and, apparently, in blue-green algae. Although our primary interest was in the existence of phycobilisomes, we also made observations on polyhedral and other structured bodies in the blue-green algae examined. 1 Published with the approval of the Secretary of the Smithsonian Institution. MATERIALS AND METHODS Cultures. Anacystis nidulans was obtained from J. Myers of the University of Texas. Cultures were grown in liquid medium D, as described by Kratz and Myers (14). The cultures were illuminated with light from incandescent lamps with an incident illumination of 150 ft-c. Tolypothrix tenuis was obtained from M. Gibbs at Brandeis University, and Fremyella diplosiphon from M. Krauss at the University of Delaware. The medium for these algae was that employed by Hattori and Fujita (11). The cultures were grown in liquid or on agar under cool, white fluorescent light (150 ft-c) at room temperature. An unidentified oscillatorialike marine blue-green alga was grown under the same conditions as T. tenuis and F. diplosiphon, except that the medium used was an artificial seawater medium described by Jones et al. (12). Electron microscopy. The cells were fixed in 4% glutaraldehyde in 0.1 M phosphate buffer (ph 6.8) for 1 to 2 hr. The cells were usually rinsed in the buffer prior to fixation. Occasionally, the glutaraldehyde was added directly to the medium. Similar results were obtained with both procedures. Postfixation was in 1% osmium tetroxide (in 0.1 M phosphate buffer, ph 6.8) for 2 to 2.5 hr. The embedding and staining procedures were the same as those previously described (7). For negative staining, A. nidulans cells were exposed to brief sonic treatment (30 to 45 sec at an output of about 30 d-c amp in a Branson Sonifier (Branson Instruments, Inc., Stamford, Conn.). Then they were immediately applied to Formvar carbon-coated grids and stained with 1% phosphotungstic acid (ph 7.2). 1486
2 VOL. 97, 1969 ULTRASTRUCTURE OF BLUE-GREEN ALGAE 1487 RESULTS The ultrastructures of T. tenuis and F. diplosiphon are very similar. The cells of these filamentous algae differ primarily in shape; T. tenuis is more elongated and F. diplosiphon more bulbous. The overall structure of both is not unlike that of the vegetative cell of Nostoc (15). Cells are enclosed by the typical wall layers, as described by Jost (13), and each filament is normally surrounded by a fibrous gelatinous sheath. The sheath is quite thick in older cells, but it is thin or absent (perhaps as a result of treatments involved in fixation) in young cells. In both Fremyella and Tolypothrix, older cells are characterized by extensive amounts of carbohydrate storage products. These storage products, named a-granules by Pankratz and Bowen (17), obscured most of the small internal detail; therefore, it was necessary to concentrate on young cells in our investigation. Figure 1 represents a young vegetative cell of F. diplosiphon, and Fig. 2, a section of T. tenuis. Within each cell, the photosynthetic lamellae are randomly arranged and interspersed with several nuclear areas. Interlamellar spaces and numerous darkly staining bodies, which may be small structured granules or osmiophilic bodies, are common in young cells. The interlamellar spaces are absent in older cells of the same preparations, whereas the number of darkly staining bodies is smaller. The lamellae, each consisting of a membrane pair, have small electron-dense granules (20 to 35 nm in diameter) attached to one surface (Fig. 1, 2). By analogy from our work on P. cruentum (9), these granules are regarded as phycobilisomes. Phycobilisomes are characterized by containing phycobiliproteins and being directly attached to one side of the photosynthetic membranes, i.e., on the side facing away from its own membrane pair. Furthermore, they are oriented in evenly spaced rows on the lamellae. A suggestion of the parallel rows can be seen in Fig. 1 and 5. Phycobilisome rows on facing membranes can be directly opposite one another (as in some areas of Fig. 2), or they can have an alternate arrangement (Fig. 1, 2,4, 5). As anticipated, phycobilisomes were found in both freshwater (Fig. 1, 2) and marine blue-green algae (Fig. 4, 5). The organism shown in Fig. 4 and 5 was isolated from a marine aquarium. Inasmuch as this organism has a filamentous nature whose individual filaments are normally surrounded by a fibrous sheath, and because it has characteristic oscillations as observed under a light microscope, it is regarded as oscillatorialike. From spectrophotometric readings on aqueous extracts, it was determined that this alga has phycocyanin as its accessory pigment, and that it lacks phycoerythrin altogether, whereas T. tenuis and F. diplosiphon have both phycobilins. When the plane of section passes perpendicular to the rows of phycobilisomes, the individual aggregates can be most clearly seen. In the boxed area of Fig. 4, the regular spacing on the lamellae is obvious. As the lamellae are sectioned diagonally, the phycobilisome shape changes from the broad-face view to the longitudinal view. When the plane of section is parallel to the rows, they appear only as rather indistinct segmented bands of somewhat greater electron density (Fig. 5) than the surrounding material. Phycobilisomes were not observed in A. nidulans (Fig. 6, 7). Polyhedral bodies are apparently ubiquitous in all blue-green algae and were certainly present in all four species we examined. Although our main interest was in the phycobilisomes, some structural characteristics of the polyhedral bodies seemed worth noting, especially those in A. nidulans. Regardless of the species, the polyhedral bodies were always in the nucleoplasm (Fig. 1, 2, 4-8), adjacent to ribosomes and to fibrils, which are generally assumed to contain deoxyribonucleic acid. Although there sometimes is a definable interface (Fig. 9), limiting membranes were not observed around the polyhedral bodies. The figures show the considerable variation in the size and shape of the polyhedral bodies. Only in cells of A. nidulans have we ever observed such long polyhedral bodies as that illustrated in Fig. 7. In 3-week-old cultures, under our growth conditions, it was not uncommon to find that one polyhedral body spanned the length of two cells. The polyhedral bodies appeared to be quite rigid since they were always straight and in several cells seemed to retard or prevent completion of cell division. Inasmuch as these polyhedral bodies were known to have a regular shape, as their name implies, it was not surprising to find that they possessed a highly ordered structure. Upon close examination, one can observe a periodicity with a helical pitch (Fig. 8). By negative staining (Fig. 9), it was possible to show that the periodicity is due to the regular arrangement of equal subunits which causes the crystalline-type structure of the polyhedral bodies. It should be pointed out that the periodicity was not always helical; sectioned material sometimes revealed a periodicity parallel with the long axis of the body. In addition to the polyhedral bodies and what appeared as small structured granules (Fig. 2, 3a), cells of T. tenuis possessed a third type of structured body. In Fig. 3a, a segmented rod is seen to pass through the cell. The enlargement in Fig. 3b
3 O#_W W w n t X s t < s ~~~~~~~~~et 1488 GANIT AND CONTI J. BACTERIOL. I \ W Su t LI- X_ ; _ N. I *K ".1 _a,._w 4 'tx.- CF7. 4S r VW.'p.. : 1 o tr f., x, A;'es- -wt, '- L:s>-;': eva '. *r,l1 AL-T tv *0 4 is.f. t 4 # P-.,;ffiS}>en!TW psr m 6S ) FIG. 1. Section of F. diplosiphon with nuclear areas containing several polyhedral bodies (Pb). Phycobilisomes are evident as small dark-staining granules attached to the lamellae. The interlamellar spaces are characteristic of young cells, as are the dark-staining spherical bodies. The arrows indicate a lamellar area where faint traces of the parallel phycobilisome rows are present. X 37,800. Bar indicates 0.5 jum.
4 VOL. 97, 1969 ULTRASTRUCTURE OF BLUE-GREEN ALGAE 1489 FIG. 2. Section from a cell of Tolypothrix tenuis. Phycobilisomes (arrows) are present on the photosynthetic lamellae. Note the polyhedral body (Pb) and the clearly defined plasma membrane (arrow heads). The dark bodies at the cell junction are probably small structured granules or osmiophilic bodies. A gelatinous sheath (not shown here) normally surrounds older cells. X 78,000. Bar indicates 0.5 jsm. reveals that the rod is composed of stacked discshaped units, each of which has an electron-dense center and a less dense outer coat. In the middle region of Fig. 2b a grazing section can be seen over the outer portion of the subunits where the electron-dense center is absent. Although most of these structured bodies were rod-shaped, some assumed a horseshoe shape. The nature and function of this structure is unknown; its appearance suggests an aggregation of virus particles, but there was no evidence of virus infection or cell lysis.
5 - _ I!wF 41= C FIG. 3. Sections of Tolypothrix tenuis. (a) A large structured body of unknown function traverses the cell. X 41,000. Bar indicates 0.5,m. (b) Enlargement of the structured body seen in 3a. Note the periodicity and the electron-dense center. The absence of the darker staining core in the middle of the photomicrograph represents a more lateral section of the rod-shaped body. X 155,000. Bar indicates 0.1 pm. FIG. 4. Phycobilisomes in a marine blue-green alga. Their even spacing on the lamellae can be seen within the boxed area. X 74,000. Bar indicates 0.5,um. 1490
6 VOL. 97, 1969 ULTRASTRUCrURE OF BLUE-GREEN ALGAE 1491 Downloaded from FIG. 5. Tangential section of a filamentous marine blue-green alga. Two views of the phycobilisomes are present on the lamellae. In the lamellar area on the right, the phycobilisomes are seen in cross section. Ifone traces the lamellae toward the top left, phycobilisome rows evolve and appear as more darkly staining segmented bands. Polyhedral bodies (Pb) are present in the center oftcze cell. X 81,000. Bar indicates 0.5,m. DISCUSSION Even though phycobilisomes have not as yet been isolated from blue-green algae, we felt justified in assuming that the granules attached to the lamellae (Fig. 1, 2, 4, 5) are equivalent to those seen in red algae (7-9). Since both algal groups possess phycobiliproteins as accessory pigments, and because their lamellar arrangement is essentially the same (grana or face-to-face fusions of adjacent lamella are absent), it is certainly plausible that they both possess phycobilisomes. Phycobilisomes are clearly aggregates of phycobiliproteins, but it is not known whether the entire phycobiliprotein content is present within them. Experiments using T. tenuis and F. diplosiphon are now in progress to establish whether the shape of the phycobilisomes in the blue-green algae is determined by the predominant phycobiliprotein present, as seems to be the case in P. cruentum and Porphyridium aerugineum [with spherical and on February 27, 2019 by guest
7 Downloaded from of efi " #u.v 4si j, on February 27, 2019 by guest FIG. 6. Ultrastructure ofa representative cell ofa. nidulans. Six densely staining polyhedral bodies are present in the central region (nucleoplasm); they are surrounded by ribosomal particles andfine fibers, generally believed to contain deoxyribonuclekic acid. Four lamellae are present along the cellperiphery. The carbohydrate storage products appear black between the lamellae. Phycobilisomes are not visible. X 55,000. Bar indicates 0.5,m. FIG. 7. In this dividing cell, as noted by the invagination of the lamellae and the wall layers, a very long polyhedral body extends across both potential daughter cells. X 44,000. Bar indicates 0.5 jam. 1492
8 VOL. 97, 1969 ULTRASTRUCTURE OF BLUE-GREEN ALGAE 1493 disc-shaped phycobilisomes, respectively; (10)]. When the cultures are grown under red light, phycocyanin production predominates; under green light, phycoerythrin is produced in excess of phycocyanin. In this way, the possible relationship between phycobilisome shape and relative pigment content will be studied. The limiting factor at present is the lack of consistent excellent preservation of the phycobilisomes. The difficulty in preservation ofphycobilisomes is thought to be the cause for their apparent absence in A. nidulans. Although the general ultrastructure of this alga has been well illustrated by Ris and Singh (18) and Allen (1, 2), their illustrations show no evidence of phycobilisome-type structures. Phycobilisomes in blue-green algae have only been reported once in the literature. Although Lefort (16) did not identify the structures as phycobilisomes until later (3), she nevertheless showed them on the lamellae of two blue-green endosymbionts, Glaucocystis nostochinearum and Cyanophora paradoxa. Furthermore, she was unable to find them in free-living blue-greens. Aside from this report, we are aware of three other species in which phycobilisomes have been observed; Synechococcus (M. R. Edwards et al., J. Phycol., in press), Plectonema, and Nostoc (M. R. Edwards and J. Reese, personal communication). We expect that phycobilisomes are present in all algae (Cyanophyta, Rhodophyta,and Cryptophyta) where phycobiliproteins are present as accessory pigments. The reason phycobilisomes have not been more commonly observed is believed to be due to the difficulty in preserving them for electron microscopy. Preservation of phycobilisomes in free-living blue-green algae is rather random, similar to the problem encountered in preserving chloroplast ribosomes. The problem is not encountered with preservation of cytoplasmic ribosomes. From our observations, it is clear that the polyhedral bodies, or "crystalline bodies" as Wildon and Mercer (19) call them, are composed of small units in an orderly array. The crystalline arrangement suggests that the units are of a regular size and perhaps of the same nature. Unfortunately, to our knowledge, the chemical composition of the polyhedral bodies is not known. Our limited experience suggests that their FIG. 8. Clear helical periodicity is present in the longitudinally sectioned polyhedral body. X 176,000. Bar indicates 0.1,um. FIG. 9. Subunits are evident in this top view ofa polyhedral body stained with 2% solution of sodium phosphotungstate. Note evident periodicity. X 250,000. Bar indicates 0.1,um. isolation will not be a problem and that their general chemical nature could easily be determined. ACKNOWLEDGMENTS This investigation was supported by Atomic Energy Commission grant AT(30-1)-3913 and by National Science Foundation grant GB We would like to thank K. M. Towe (Paleobiology Department, Smithsonian Institution) for the use of the Philips EM-200 and associated facilities. LITERATURE CITED 1. Allen, M. M Photosynthetic membrane system in Anacystis nidulans. J. Bacteriol. 96: Allen, M. M Ultrastructure of the cell wall and cell division of unicellular blue-green algae. J. Bacteriol. 96: Bourdu, R., and M. Lefort Structure fine, observee en cryode capage, des lamelles photosynthetiques des Cyanophycees endosymbiotiques: Glaucocystis nostochinearum Itzigs, et Cyanophora paradoxa. Compt. Rend. 265: Duysens, L. N. M Transfer of light energy within the pigmnent systems present in photosynthesizing cells. Nature 168: Echlin, P., and I. Morris The relationship between blue-green algae and bacteria. Biol. Rev. Cambridge Phil. Soc. 40: French, C. S., and V. K. Young The fluorescence spectra of red algae and the transfer of energy from phycoerythin to phycocyanin and chlorophyll. J. Gen. Physiol. 35: Gantt, E., and S. F. Conti The ultrastructure of Porphyridium cruentum. J. Cell Biol. 26: Gantt, E., and S. F. Conti Granules associated with the chloroplast lamellae of Porphyridium cruenttum. J. Cell Biol. 29: Gantt, E., and S. F. Conti Phycobiliprotein localization in algae, p In Energy conversion by the photosynthetic apparatus. Brookhaven Symp. Biol. no Gantt, E., M. R. Edwards, and S. F. Conti Ultrastructure of Porphyridium aerugineum a blue-green colored rhodophytan. J. Phycol. 4: Hattori, A., and Y. Fujita Formation of phycobilin pigments in a blue-green alga, Tolypothrix tenuis, induced by illumination with colored lights. J. Biochem. (Tokyo) 46: Jones, R. F., H. L. Speer, and W. Kury Studies on the growth of the red alga Porphyridium cruentum. Physiol. Plantarum 16: Jost, M Die Ultrastruktur von Oscillatoria rubescens. Arch. Mikrobiol. 50: Kratz, W. A., and J. Myers Nutrition and growth of several blue-green algae. Am. J. Botany 42: Leak, L. V Electron microscopic autoradiography incorporation of H3-thymidine in a blue-green alga, Anabaena sp. J. Ultrastruct. Res. 12: Lefort, M Sur le chromatoplasma d'une cyanophycde endosymbiotique: Glaucocystis nostochinearum Itzigs. Compt. Rend. 261: Pankratz, H. S., and C. C. Bowen Cytology of bluegreen algae. L. The cells of Symploca muscorum. Am. J. Botany 50: Ris, H., and R. N. Singh Electron microscope studies on blue-green algae. J. Biophys. Biochem. Cytol. 9: Wildon, D. C., and F. V. Mercer Ultrastructure of the vegetative cell of blue-green algae. Australian J. Biol. Sci. 16:
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