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Ultrastructural Studies on the Blue-Green Algal Symbiont in Korschikoff

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Ultrastructural Studies on the Blue-Green Algal Symbiont in Korschikoff ULTRASTRUCTURAL STUDIES ON THE BLUE-GREEN ALGAL SYMBIONT IN CYANOPHORA PARADOXA KORSCHIKOFF WILLIAM T. HALL, Ph.D., and GEORGE CLAUS, D.Se. From The Rockefeller Institute and New York University Medical Center, New York ABSTRACT Studies conducted on the ultrastructurc of Cyanophoraparadoxa Korschikoff (a cryptomonad) have shown that its intracellular symbiont is closely related to unicellular blue-green algae. Due to its peculiar habitat, the intracellular symbiont lacks the characteristic cyanophyccan double-layered cell wall, but is surrounded by a thin protoplasmic membrane. The proto- plasm itself is differentiated into a lamellated chromatoplasm containing photosynthetic pigments, polyphosphate granules, and possible oil droplets, and a non-lamellar centro- plasm with a large centrally located electron-opaque body surrounded by a fibril-containing halo. 2-his halo-central body complex may be nuclear in nature. Binary fission of the or- ganism is described. Since this cyanelle has not yet been classified, we name it Cyano- cyta korschikofftana nov. gen. nov. sp.; and because of its structural peculiarities, we find it necessary to create a new family for it, Cyanocytaceae, in the order Chroococcales. INTRODUCTION With the term "Syncyanosen," Pascher (1914) that organism found within the flagellate Cyano- described the general phenomenon of a blue-green phora paradoxa Korschikoff (Fig. 1). Although this alga living symbiotically with a colorless protist. intracellular symbiont is one of the most In his paper, he reported cases in which the cyano- thoroughly studied of the cyanelles ("Cyanellen"-- phyte was attached on the external surface of the Pascher, 1929), its nature still remains a paradox. host organism. In 1924, Korschikoff published a Investigators since Korschikoff point out the great description of a flagellate containing in its proto- similarity of the organism to blue-green algae. plasm colored bodies which bore a striking resem- However, Geitler (1959) enumerates several blance to unicellular blue-green algae. In spite of arguments against this conventional theory. His this similarity, he himself expressed doubt about main points are the following: (1) the negative their cyanophycean nature and supposed that he response of the inner body to nuclear stains even had found an organism sui generis. With an when using a special technique developed by accumulation of reports on symbiotic blue-green Lietz (1951); (2) the possibility of separating algae, some occurring within the host's protoplasm, the inner body from the isolated cyanelles with- others on its external surface, Pascher (1929) dis- out causing any apparent damage; (3) the tinguished between "Endocyanosen" and "Ecto- absence of an ergastic membrane (wall?) around cyanosen." the organism which thus permits swelling with- In the present paper, we wish to deal with the out rupturing, contrary to observed blue-green internal type of relationship and in particular with algal responses; and (4) the prolonged existence 551 of the division-furrow, which characteristically patterns were placed on 300-mesh bare grids. Sections is a transient feature of normal cyanophycean were stained with PbOH using the method of division. In an attempt to clairfy the issue we Feldman (1962) and were observed under a Philips EM 100B. have undertaken a complementary light- and electron-microscope study. RESULTS Since, to our knowledge, the cyanelles of the species of the Cyanophora Korschikoff genus were Cyanocyta korschiko~ana, a more or less spherical never named, we propose the following generic body with diameter of 1.5 to 3.7 micra, is randomly and specific name to designate the specimens de- distributed throughout the protoplasm of the host scribed below: Cyanocyta korschikofliana nov. gen. flagellate. The number of these bodies present in nov. sp. any single host organism varies from one to several, The host organism will be described in detail usually 4 to 6. Their bluish-green color is restricted elsewhere. to a peripheral zone, whereas in their center, a usually spherical, but sometimes irregularly MATERIALS AND METHODS shaped, seemingly colorless area is visible. Between Culture material was obtained through the courtesy the chromatoplasm and the more refractile central of Dr. Luigi Provasoli (Haskins Laboratories, New area, a less refractile thin halo is discernible. After York) from the original isolate of Pringsheim (1958). Feulgen staining (repeated in five different experi- Both of these investigators accepted the cultures as ments), the halo area turned magenta, whereas the Cyanophora paradoxa Korschikoff, although the flagel- chromatoplasm could be observed as an unstained late usually contains more than two cyanelles, which surrounding capsule. Only the nuclei of the host is the characteristic number originally reported by flagellates showed any positive response to the Korschikoff. A second species, C. tetracyanea, reported Feulgen treatment. A species of Oocystis admixed to by Korschikoff in 1941, contains, as the name sug- gests, four cyanclles, whereas the flagellates in the ma- the culture served as an internal control for the terial we investigated occasionally possessed as many staining. In this case also, only the nuclei of the as nine. Therefore, the identity of the flagellate com- green alga gave a positive reaction. These results ponent of the symbiosis is questionable. would indicate that chromatin material is con- Feulgen staining was performed according to the tained within the halo-central body complex of the method of Conn (1953). An ortholux phase contrast intracellular symbiont. To what extent, if any, the microscope with 70 and 90 X oil immersion objectives actual central body responds to the Feulgen stain and 10 and 25X oculars was employed. cannot be determined because the stained halo For electron microscope investigations, ultrathin impedes investigation of the core. sections were prepared. The material was centrifuged The division of is apparently at 1000 RPM for 10 minutes until a pellet was formed. C. korschikojfiana This was cut into small pieces, fixed in phosphate- independent of the division of its host, and the buffered (pH 7.2) 1 per cent osmium tetroxide for 1 cyanelles are not necessarily equally distributed to hour, dehydrated through a series of alcohol concen- the resulting daughter cells of the host. The furrow trations, put into propylene oxide for 20 minutes, and frequently observed on their surface is a centripe- then transferred into a 1:1 propylene oxide-Epon tally progressing division furrow which invariably mix, which was placed in an oven at 57°C. for 2 results in the production of two daughter cells, hours. To assure better infiltration, the material was although it may temporarily lag in the process. then put into pure Epon and allowed to stand over- Ultimately, the central body is cleaved by the in- night at room temperature before it was placed in vaginating furrows. capsules and finally embedded in Epon, which was Ultrastructurally, shows a thin allowed to harden for 2 days at 57°C. The Epon was C. korschikofiana mixed in the following proportions; limiting membrane directly apposed to a proto- Epon 812 100 ml. plasmic membrane of the host (Figs. 1 to 3). DDSA 1 180 ml. The algal limiting membrane is visibly thicker HHPA 10 ml. than the lamellar membranes (Fig. 3) and in some BDMA 3 ml. cases appears to be double. Pores were not ob- Sections were made with a glass knife on a Porter- served in this membrane, nor could a direct con- Blum microtome and those showing gray interference nection with the cytoplasmic lamellae be detected. 1 DDSA : dodecenylsuccinic anhydride. The chromatoplasm, readily discernible in the HHPA: hexahydrophthalic anhydride. light microscope by its blue-green color, is equally BDMA: benzyldimethyl amine. distinctive in the electron microscope. Composed 552 THE JOURNAL OF CELL BIOLOGY • VOLUME 19, 1963 Figures 1 to 19 are all electron micrographs. I~OURE 1 Section showing the flagellate, Cyanophora paradoxa, with two blue-green algae lying in the cytoplasm. There seems to be no particular pattern of distribution, though when several algae are present they often are in close proximity to the nucleus of the host. )< ~0,000. of more or less concentric lamellae and inter- labyrinthine pattern, the ground substance of the lamellar spaces, the area presents an abrupt con- central body halo is in contact with that of the trast to the non-lamellated centroplasmic area interlamellar spaces and presumably miscible (Fig. 4). Because the lamellae are not perfectly with it (Figs. 4, 6, 7). concentric, but seem rather to form an interrupted The lamellae themselves are double-membraned WILLIAM T. HALL AND GEORO~ CLAUS Ultrastructur8of Blue-Green Algal Symbiont 553 structures, 175 to 200 A thick, with a total period since the~ are thinner than the lamellae they may from one lamella to the next of about 400 A. Their be sectioning artefacts rather than true bridges. distribution is reminiscent of the orderly mem- The centroplasm can be divided into two por- brane arrangement exemplified by Osdllatoria tions, a rather electron-opaque central body sur- chalybea Mertens (Hall and Claus, 1962) (Fig. 5). rounded by a less dense halo which possesses Along the lamellar membrane there is a more or fibrillar strands extending from the fringe of the less uniform distribution of small electron-opaque lamellae up to and, perhaps, into the central particles, probably the chlorophyll content of the body (Fig. 7)i In their structure, these fibrillar cell (Fig. 3). In some areas along the membrane, elements of the halo are rather similar to the fine the intralamellar spaces widen to form small fibrillar elements of the nucleoplasm described in vesicles (Fig. 9) of the type previously observed blue-green algae by Ris and Singh (1961) and occurring regularly in O. chalybea. Hopwood and Glauert (1960), and they prob- The space between lamellae is about twice the ably represent the chromatin material of the or- width of the lamella and is filled with a finely ganism.
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