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Ultrastructure of Endosymbiotic Chlorella in a Vorticella

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Ultrastructure of Endosymbiotic Chlorella in a Vorticella DNA CONTENTOF DOUBLETParamecium 207 scott DM, ed., Methods in Cell Physiology, Academic Press, New cleocytoplasmic ratio requirements for the initiation of DNA repli- York, 4, 241-339. cation and fission in Tetrahymena. Cell Tissue Kinet. 9, 110-30. 27. ~ 1975. The Paramecium aurelia complex of 14 30. Yao MC, Gorovsky MA. 1974. Comparison of the sequence sibling species. Trans. Am. Micrnsc. SOL. 94, 155-78. of macro- and micronuclear DNA of Tetrahymena pyriformis. 28. Woodward J, Gelher G, Swift H. 1966. Nucleoprotein Chromosomn 48, 1-18. changes during the mitotic cycle in Paramecium aurelia. Exp. Cell 31. Zech L. 1966. Dry weight and DNA content in sisters Res. 23, 258-64. of Bursaria truncatella during the interdivision interval. Exp. Cell 29. Worthington DH, Salamone M, Nachtwey DS. 1975. Nu- Res. 44, 599-605. J. Protorool. 25(2) 1978 pp. 207-210 0 1978 by the Socitky of Protozoologists Ultrastructure of Endosymbiotic Chlorella in a Vorticella LINDA E. GRAHAM* and JAMES M. GRAHAM? “Department of Botany, University of Witconsin, Madison, Wisconsin 53706 and +Division of Biological Sciences, University of Micliigan, Ann Arbor, Michigan 48109 SYNOPSIS. Observations were made on the ultrastructure of a species of Vorticella containing endosymbiotic Chlorella The Vorticella, which were collected from nature, bore conspicuous tubercles of irregular size and distribution on the pel- licle. Each endosymbiotic algal cell was located in a separate vacuole and possessed a cell wall and cup-shaped chloroplast \\ith a large pyrenoid. The pyrenoid was bisected by thylakoids and surrounded by starch plates. No dividing or degenerat- ing algal cells were observed. Index Key Words: Vorticella; Chlorella; symbiosis; ultrastructure. YMRIOTIC relationships between algae and aquatic inver- cluded that the specific identity of these 2 putative species must S tebratcs have long been of interest, and a number of excellent be established on grounds other than intracellular zoochlorellae, reviews are available (2, 5). Ochsman (8) pointed out that because the stability of the symbiotic relationship was in doubt. the ultrastructural study of these symbiotic associations is useful With the exception of a report of some unpublished observations in determining the host-symbiotc interface, the influencc of the by Ochsman (8), the ultrastructurc of vorticellids containing invertebratc host on symbiote structure and reproduction, mor- algal cndosymbiotes has not bcen previously studied. In the phologic evidence for movement of nutrients between organisms, present report the fine structure of a green Vorticella is com- and evidence of the ability of the host to digest thc symbiotes. pared with that of H. viridis (8) and P. bursaria (4) with ln frcsh-water hosts, zoorhlorellac of the genus Chlorella are the particular attention to the relations bctwecn host and symbiote most common symbiotic algae, and they have been observed in discussed by Ochsman (8). Although the focus of this papcr is a number of protozoan genera (2, 5). Ultrastructural studies of not taxonomic, a brief description of the dimensions and features endosymbiotic Chlorella have been reported for Hydra viridis of the green Vorticella studied by light microscopy will also br (8) and Paramecium bursmia (4), and research on these 2 given. symbiotic assoriations has recently been summarized (3, 6). Thesc studies have contributed substantially toward an under- MATERIALS AND METHODS standing of the relationships mentioned by Ochsman (8) for Repeated collections of a grcen Vorticella were made in a fresh watcr endosymbiotic associations, but more such studies pond on the Loesell Field Laboratory of Eastern Michigan Uni- arc needed (4). versity in Ypsilanti, Michigan. This Vorticella typically oc- Zoochlorellae have bcen infrequently reported in the fresh curred in large groups which were easily seen as bright green, Lvatrr ciliati. Vorticella. In their taxonomic rcvicw of this genus irregularly shaped macroscopic patches on the undersides of old n’oland & Fin1c.y (7) reported that zoochlorellae wcre observed floating leaves of Nuphar, on submerged leaves of Spnrganium, in the putative specirs Vorticella chlorostigma Ehrenberg, and and on roots of Spirodela. Pieces of leaves bearing L70rticella T~’ovticcl1a fascirulata 0. F, Muller. Noland & Finley (7) con- patches were excised, fixed overnight in 2% (v/v) glutaralde- + Fig. 1. Photomicrograph of a single green Vorticella. Note the stalk (ST) as well as the distribution of algae and pellicular tuber- cles (arrow). Bright field, axial illumination. X800. Figs. 2-4. [Electron micrographs of ultrathin sections through various parts of green Vorticella.I 2. An endosymbiotic Chlorella is seen in a perialgal vacuole situated near the contractile vacuole (CV). The cup-shaped chloroplast (C) of the alga contains a pyrenoid (P) bisected by thylakoids and surrounded by small starch plates X15,800. 3. Sections of the infundibulum (IN) con- tain intact bacteria, while bacteria in various stages of digestion are evident in food vacuoles (FV). Lysosome-like bodies (LY) are near the food vacuoles. x6,300. 4. Spasmoneme (SP) and bgtonnets (B) are seen in a cross-section of a ciliate’s stalk. x8.300. Figs. 5, 6. [Electron micrographs of cross-sections of green Vorticella.1 5. Near the adoral end of the ciliate, note sections of vestibulum (VE) and pellicular tubercles (T), which contain electron-dense material. X 5,700. 6. Near the aboral end basal bodies (EB) mark a part of the trochal band. Four algae are lodged in perialgal vacuoles with apposed membranes (arrows) ; these cells may be the products of a recent division. Note also a part of a food vacuole (FV) and the lysosome-like bodies (LY). x8,600. 209 hyde in 0.05 ni cacodylatc huffrr at pH 7.3, \\-;irli(,d ivith buffer, .;;!.inbiotic Chlorc~llaniay be rclated to its capability for indepen- fixed with 2% (w/vj OsO, in the same lmffrr, and \\-ashed dent existencr or, as Karakashian ct al. (4) suggested, the in- again with buffrr. The sprcimens \\-err then stained en bloc for cornpletcncss of adaptive changes of Chlorclla to symbiosis. As 15 niin in 0.5% (iv/v) aqwous uranyl ac it?, ctch!-dratrcl in in P. bici-saria and H. rriridis the symbiotic Chlorella in Vorticclla an ethanol wries, and cnihcddecl in Epon i 1 1 ) ~ using prop! Ir-nc h:r\~21 aingli. cup-shaped chloroplast. The pyrenoid of the alga oxide as a transitional solvrnt. Swtions \\-err cut on 3x1 I,BK in 170rticclln is veq siniilar to that in P. bursaria. Pyrcnoids Ultratome equipped xvith :I diamond knifc. stained briefly Ivitli wrr aliscnt from the CAL strain of H. uiridis (8), although lead citrate (lo), and esaniinrd in an R<:r\ EAfU 3G elt~tron the,!- ~vrrrpriwnt in the other 2 strains examined. microscope operated at 50 k\-. Thr 1irotozo;i \\-?re orienicd in Thc, algal symhiotc~s of Vorticclln, like those of P. bursaria the blocks so that cells \vcrc approximately cross-swtioncd. Scc- ;4) and H. riridis (8),lie singly in pcrialgal vacuoles (4). In tions wrre made of at least 10 individuals. I-’. hu)-snvia Karakashim ct al. (4) commonly found algae under- goinq dig-cstion in food Lwxioles along with bacteria, but in RESU LTS culture, P. hursnria continuously releases Chlorrlla into the Each grren b70rtirr//n \\as att;ic.licd to thr, Iwf substratc by medium \\ here they can be iiigrstcd by the ciliates. Since the an unbranched, spirally contractilv stalk. Typical shape. sizr, I-oI-ticrlla in this rcport uwc obtained in nature, thew was prob- and distrihution of algal c.c,lls is shown in a I)hotoinicro~ra~)liof ably less chance of ingesting algae than if these ciliates had been in cultiw. So dividitig algal cclls wcrr secn in As a singlc green Vorticrlla Fig. 1). Thc in(wi Icm~thof 10 vnr- Vorticella. in th(. caw of digestion of algae, however, their division would ticellids, cxclirding stalk, 1%as + pin, xid thc inraii \\-idth at inori~likrly br obscrvcd in rapidly multiplying laboratory cultures the \videst point of 19 vorticr s \\xs 50.4 piii. Thr cxtrndcd than in c(,Ilr isolated from nature. stalk tvas 4.4 pni \viclt. and at Icast 175 pni Ioiig. The length of There have brcn relatively few ultrastructural studies of onc coniplrtr turn of thr u~~xsii~nn~~iii~~rpiral u ;IS 29 /mi. The - s!-mbiotic Chloi-clla (4, 8). The prcsent report of the ultrastruc- pellicle tvas ornamented \\.it11 tu1)rrclrs of irrcyular sizr and distribution (Figs. 1. 5, 6). turc of cndosymbiotic. Chlorella in a species of Vorticrlla should The general ultrastnirture of thr crll body and stalk of the faditate comparison \vith other algal symbioses. The limited icrlla \\as similar to that of 170rtirclla conr,allarin oIis:cr\.ations suggest that rndosymhiotic Chlorella in diffrrent 1 1 , esccpt for tiit’ prt’scncr of pel1icul:rr tul)c*rcles iti\.cwc*liratc hmts arc u1tr:istructurally similar. Thcsr tuberclcs xccrt: found to contain rxrying amounts of an rlcctroii-d~m.;cgranular nintcrial. Intact bacterial .\C:I(rU”)~2‘LEnGEMENT cells codd Iw nhscrved in the infuiidibulurn. and degradcd ’I’lic. :iuthors uirh to thaiik Dr. R. J. Lowry for the use of his bacterial crlls Ivrrc ptxwiit in the food variioles surrounded hy t,ltv-tron microscopr facilitirs arid Allen for reviewing a single membrane (Fig. 3). Dr. S. I,. The vndosyinhiotic Chlorclln \\-crv distriliutcd throiighout thc this ninnuscript. cytoplasm nf the grren T’orticclla. Each nlgal crll !\-;is contained in a srparatc vacuolv structiiwlly siinil;rr to thr food vacuoles REFERENCES (Fig. 3). No algal cc~lls. or remnant.: of alqnl cclls. \\we ob- 1. .illen RD. 1973. Structures linking the myonemes. endo- servrd in food vacuolrs c.ontaining lxictcria. and no Iia.tcrial plasnric reticulum. and surface membranes in the contractile ciliate r’orricelln. J.
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