The fine structure of the cortical layers in Paramecium aurelia
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1 129 The fine structure of the cortical layers in Paramecium aurelia By JOHN M. STEWART and ALAN R. MUIR (From the Department of Natural History, University of Aberdeen, and the Department of Anatomy, University of Edinburgh) With 4 plates (figs, i to 4) Summary Paramecia have been cultured in 5 % iron-dextran solution for several days, but under the present experimental conditions do not appear to synthesize the iron-storage protein ferritin. High resolution electron micrographs were obtained of the outer 'pellicular' and inner 'peribasap membranes of the cortical layer in Paramecium aureiia; both membranes proved to be triple-layered unit membranes, each having two osmiophilic layers 2 to 3 m/x thick separated by a space of 3 mju.. The outer membrane of the cilium has the same structure as, and is continuous with, the pellicular membrane. This fact is thought to be of significance with regard to antigen studies. Introduction As a result of recent electron microscope studies, the pellicle of Paramecium was envisaged as being composed of two main layers. The outer layer was considered to be continuous with the membrane covering the cilium, while the 'inner layer' was considered to enclose the peribasal space, the space between the pellicle and the cytoplasm (Sedar and Porter, 1955; Ehret and Powers, 1959). However, electron micrographs taken in the course of a study on certain cytochemical aspects of P. aurelia have shown that both these layers are considerably more complex than has been generally recognized. Materials and methods The organism used in these studies was P. aurelia, variety 1, stock 60. The culture medium, an infusion of dried lettuce, was inoculated with a suspension of Aerobacter aerogenes, and the paramecia were kept in stoppered flasks containing 25 ml of this inoculated medium at 26 0 C. Since the original aim of these experiments was to examine the possibility that the iron-storage protein ferritin might be synthesized at a protozoan level, the experimental cells were cultured for several days in a 5% 'imferon' (irondextran) culture medium, transferred to 'imferon'-free medium for several days, then fixed. Other cells were cultured in media containing 5, 10, 15, and 30 y/ml of iron, in the form of ferrous sulphate, for up to 3 days, before fixation. (For the identification of ferritin in electron microscopy, see Muir, i960.) The fixative employed was 1 % osmium tetroxide in a veronal acetate buffer [Quart. J. micr. Sci., Vol. 104, pt. 1, pp , 1963.] K
2 130 Stewart and Muir Cortical layers of Paramecium at ph 7-2. After fixation for 30 min the cells were stored in 10% ethanol. Absolute ethanol was used for dehydration, before embedding in araldite or an 8:1 mixture of butyl and methyl methacrylate; the specimens embedded in araldite were more satisfactory and all the illustrations are taken from this material. Sections were cut on a Porter-Blum microtome equipped with a glass knife and were mounted on athene 483 grids without a supporting membrane. Specimen contrast was improved by staining the sections with 1% potassium permanganate before examination in an A.E.I. E.M. 6 electron microscope. Observations Under the present experimental conditions, no ferritin was detected in P. aurelia, although iron-dextran was found in the primary and secondary food vacuoles. The fine structure of the cortical layers of P. aurelia is dealt with in 5 electron micrographs, figs. 1 to 4, the terminology used being, to a large extent, that of Ehret and Powers (1959). The cortical layer of the cell is composed of a large number of 'units', in the centre of each of which lies a cilium. The base of each cilium is sunk into a pit (fig. 2, cp). Below the outer surface of each ciliary unit (apart from immediately below the cilium itself) lies a large space. This 'peribasal space' is prominent in figs. 2 and 3 (pbs). The junctions between adjacent ciliary units are indicated in fig. 2: two such units are shown in longitudinal section, measuring 174JU. across (j to/), and 1-28 fj. across 0' t0 /') These junctions correspond to the 'secondary meridians' of Pitelka (1961). The pellicle The pellicle, the outermost limiting zone of the cell, is composed of two main membranes: an outer 'pellicular' membrane and an 'inner' membrane which is actually part of that membrane lining the peribasal space. Where these two membranes lie adjacent to one another, the space between them varies from 4 mju. to 19 m/it (fig. i,pm, iprri). However, it is also clearly seen from this figure that both the pellicular membrane and the peribasal membrane are in themselves made up of two distinct osmiophilic layers, with an intervening clear space. These osmiophilic layers of the pellicular and peribasal membranes are each 2 to 3 m^u. thick and are 3 m/x apart: thus they resemble the triple-layered 'unit membrane' of Robertson (1959). The pellicular membrane is continuous with the cilium membrane which bounds the cilium itself (fig. 1,pm; fig. 2, cm), FIG. I (plate). Section through gullet region of P. aurelia, showing outer 'pellicular' (pm) and inner 'peribasal' {iprri) triple-layered unit membranes. The peribasal membrane lines the peribasal space (pbs), and separates it from the cytoplasm (cy) of the cell. Cross-sections of cilia (c) show cilium membranes (cm), central and peripheral fibrils (cf, pf), and ciliary extensions (e).
3 FIG. I J. M. STEWART and A. R. MUIR
4 FIG. 2 J. M. STEWART and A. R. MUIR
5 Stewart and Muir Cortical layers of Paramecium 131 while the peribasal membrane lines the peribasal space and separates it from the cytoplasm of the cell. The cilia The membrane of the cilium is also a triple-layered unit membrane, with the same dimensions as the pellicular membrane (fig. 2, pm, cm). Protuberances occur on the membrane of the cilium, and appear to be definite ciliary extensions. They do not appear to be simply parts of the membrane of the cilium which have become torn or detached during fixation or embedding. These ciliary extensions have so far only been found on cilia occurring in the gullet (fig. 1, e). The cilium marked c in fig. 1 measures approximately 335 m/x by 275 mp, in cross-section. Other workers have stated that the 'average cilium' measures 270 m/x in diameter (Sedar and Porter, 1955). Each cilium has the usual arrangement of 2 central fibrils and 9 peripheral fibrils, each of the latter being double in nature (figs. 1 to 4, A, cf, pf). In the cilium already referred to in fig. 1, each of the central fibrils is 27 m/x in diameter, whilst each of the 2 fibrils of each peripheral pair is 12 to 15 m/x in cross-section. The ciliary fibrils measured by Sedar and Porter were 15 to 20 m/x in diameter (Sedar and Porter, 1955). The arrangement of the bases of the fibrils is the same as has already been described by other workers (Sedar and Porter, 1955; Fawcett, 1961). The peripheral fibrils extend into the cell for a distance of 390 m/x below the level of the pellicular membrane (fig. 2, pm, pf), and terminate at a distance of 310 m/x below the level of the transverse partition (described below). The bases of the peripheral fibrils form what is conventionally known as the kinetosome (fig. 2, tp, k). The central fibrils terminate in a distinct swelling at the level of the pellicular membrane, and at a distance of 45 m/x distal to the transverse partition (fig. 2, cf, pm, tp). The transverse partition The transverse partitions extend completely across the bases of each of the cilia, a distance of approximately 270 mti. The partition is approximately 24 m/x in thickness. Piercing the transverse partition are the peripheral fibrils, extending from the cilium to the kinetosome. In each of the 2 ciliary bases seen in fig. 2 the peripheral fibrils are no m/x apart at the points where they pierce their respective transverse partitions. The parasomal sac The parasomal sac is a short cone-shaped depression or sac which connects the cytoplasm of the cell with the external environment. This sac passes from FIG. 2 (plate). Longitudinal section through two pellicular 'units' (j toj'), (j' to j") of P. aurelia. A cilium is seen sunk into a ciliary pit (cp), at the side of which is the opening of the parasomal sac (ps). Central and peripheral fibrils (cf, pf) of the cilium are evident, the peripheral fibrils passing through the transverse partition (tp) to form the kinetosome (k). The outer pellicular membrane (pm) and the inner peribasal membrane (ipm), which encloses the peribasal space, are visible. Mitochondria (m) are grouped near the bases of the cilia.
6 132 Stewart and Muir Cortical layers of Paramecium the ciliary pit, through the pellicular membrane, the peribasal membrane, and the peribasal space itself, to the region of the kinetosomes (Ehret and Powers, 1959). It is possible that it is the opening of the parasomal sac which is seen in figs. 2 and 3 (ps, pm, ipm, pbs). The kinetodesmal fibrils According to Metz and others (1953), each of the kinetodesmal fibrils arises in the region of a kinetosome and passes to one side of the cilium, where it is thought to join a main kinetodesmal fibre. The latter is considered to be the 'kinetodesma' seen in light microscopy. The kinetodesmal fibrils run parallel to the rows of cilia and trichocysts, and are prominent in fig. 3 (kf). The fibrils, which overlap in a 'shingle-like' fashion, do not appear to possess a periodic structure of any kind, nor are they embedded in any common matrix. Individual fibrils do not appear to be limited by a membrane in any way, and each is approximately circular when seen in cross-section (fig. 4, B, kf). At any one time and place, there are 5 fibrils overlapping one another, the total 'depth' of the 5 fibrils being 250 m/x (figs. 3; 4. *»» ) The trichocysts An unextruded trichocyst is illustrated in longitudinal section almost along its entire length of 2-8 /x in fig. 4, A. The trichocyst tip (tt) is approximately i-2 /x in length. The body, or sac, of the trichocyst (t) is 1 ju. at its widest point and is not very electron-dense, unlike the substance or substances forming the trichocyst tip (tt), and trichocyst cap (tc). The cap, or sheath, varies in width from 390 to 635 mju.. A triple-layered 'unit' membrane surrounds the trichocyst cap (tc), each layer being 3 m/x thick, and with a space of 3 m^ between the layers (figs. 3; 4, A, sm). The cap appears to be composed of longitudinal elements (as seen in fig. 4, A) whilst in fig. 3 cross-sections of these elements can be seen to surround the tip (tc, tt). Measurements indicate that the minimum space between the tip and the cap is 6 m/u, (figs. 3; 4, A, tsp). Unlike the trichocyst sheath, the tip appears to be homogeneous, and varies in width from 62 m/u. at its point to approximately 340 m/x at its proximal end. FIG. 3 (plate). Tangential section (slightly oblique), cut just below the surface of P. aurelia, showing cross-sections of cilia and trichocysts. The cilia have a limiting triple-layered unit membrane (cm), and central and peripheralfilaments (cf, pf), and each cilium is surrounded by a ciliary pit (cp). The openings of parasomal sacs (ps) are apparent at the sides of these pits. The pellicular and peribasal membranes (pm, ipm), the latter enclosing the peribasal space (pbs), surround the regions of the ciliary pits. A triple-layered unit membrane (sm) bounds the trichocyst cap (tc), which is separated from the trichocyst tip (tt) by a distinct space (tsp). The cap appears to be composed of longitudinal elements. Running parallel to the ciliumtrichocyst-cilium rows are the kinetodesmal fibrils (kf).
7 FIG. 3 ' atfe,.,- J. M. STEWART and A. R. MUIR
8 sm FIG. 4 J. M. STEWART and A. R. MUIR
9 Stewart and Muir Cortical layers of Paramecium 133 Discussion The fine structure of both the pellicular and peribasal membranes in Paramecium has not previously been described in any great detail. Their occurrence, however, has been briefly referred to by Schneider (1959). In the present work, a series of high resolution micrographs allowed a closer scrutiny of these membranes, and it was found that structurally they have a close resemblance to the triple or 'unit' membrane existing in numerous tissues of higher animals, and described in detail by Robertson (1959). It is of interest and significance that an apparently similar membrane structure should exist at protozoan and metazoan levels. The triple nature of the membrane of the cilium is, on the other hand, a widely accepted fact, although several workers depict this structure in their micrographs without comment (e.g. Sedar and Porter, 1955, working with P. multimicronucleatum, figs. 4 and 6; and Roth, 1958, working with P. aurelia, fig. 9). It is commented upon, however, by Roth, who demonstrated the triple 'unit' structure of the cilium membrane of Euplotes (Roth, 1956, fig- 5). The fact that the pellicular and cilium membranes are continuous is of significance with regard to antigen studies. Antigens of Paramecium concerned in the immobilization reaction have been shown to coat the entire surface of the organism, including the cilia (Beale, 1959), and it may be that the pellicular and ciliary membranes, since they have identical constituents, promote the synthesis of identical antibodies. The double structure of the peribasal membrane is illustrated in the work of Ehret and Powers, although no mention is made as to its occurrence (Ehret and Powers, 1959, fig. 5, B). A close resemblance is borne by the ciliary extensions (e in fig. 1) to the extensions described by Roth (1956) between the cilia of a cirrus in Euplotes. Roth has suggested that these interciliary extensions 'contribute to the functional unity of the cirrus' or perhaps serve to increase the absorptive or secretory surface. It may be that in Paramecium the cilia in the gullet, which in the present study are the only cilia so far found to have these extensions, are particularly well 'organized' and synchronized, and that this depends in part on their interciliary extensions. From the present study it would appear that the 'transverse partitions' at the bases of the cilia lie alongside part of the peribasal membrane. In doing so, FIG. 4 (plate) A, trichocyst of P. aurelia in longitudinal section, showing the cap (tc), bounded by a triple-layered unit membrane (im). There is a distinct space (tsp) between the cap and the tip (tt): the cap again seems to comprise longitudinal elements. The body, or sac, of the trichocyst (t) is also seen. A mitochondrion (m) and a cross-section of a cilium with its central and peripheral fibrils (cf, pf) are also in the picture. B, longitudinal section, showing 'shingle-like' arrangement of kinetodesmal fibrils (kf) in P. aurelia. Also seen are the pellicular and peribasal membranes (ptn, iptn), the latter enclosing the peribasal space (pbs), a trichocyst tip (tt) surrounded by its cap (tc), and mitochondria grouped near the surface of the cell (>«).
10 134 Stewart and Muir Cortical layers of Paramecium the transverse partition may possibly form a 'seal' between the cellular cytoplasm and the cilium. The only structures piercing the partition are the pairs of peripheral fibrils. In Euplotes the central fibrils also pass through the transverse partition (Roth, 1956). Thus the transverse partition could conceivably serve a double function: it could, as has been pointed out, effectively seal off the cilium from the rest of the cell, and it may possibly also serve as a point for leverage for the movement of the ciliary fibrils. The relationship of the transverse partition to the cilium requires further investigation. The shingle-like arrangement of the kinetodesmal fibrils as seen in transverse and longitudinal sections in the present study, confirms previous findings for Paramecium (Metz and others, 1953; Sedar and Porter, 1955), although other workers, also using Paramecium, have demonstrated in addition a typical spiral arrangement (Ehret and Powers, 1959). With the methods used in the present study, no transverse or periodic structure could be detected in the kinetodesmal fibrils, as has been described by other workers using P. multimicronucleatum (Sedar and Porter, 1955). It can be seen clearly from fig. 4, A that the trichocyst cap is covered by a triple unit membrane, not by a single membrane as previously described (Sedar and Porter, 1955)- The same workers demonstrate a number of small dense granules lying in the space between the tip and the cap of the trichocyst in P. multimicronucleatum. Such granules could not be demonstrated in the present study with P. aurelia, but it may be that a species difference accounts for this or, more simply, the different techniques used. We are indebted to Dr. G. H. Beale, F.R.S., for his helpful criticism and advice regarding this work, and to Dr. L. L. de Kock and Dr. D. R. Pitelka both of whom read and criticized the manuscript. The electron microscope, which is on permanent loan from the Wellcome Foundation, was maintained by Mr. G. Wilson. Other technical help was provided by Mr. R. McDougal and Mr. A. E. G. Dunn. One of us (J. M. S.) is a Medical Research Council postgraduate student. References BEALE, G. H., Proc. R. phys. Soc. Edinb., 28, 71. EHRET, C. F., and POWERS, E. L., Int. Rev. Cytol., 8, 97. FAWCETT, D., In The cell, edited by Bracbet and Mirsky, 2, 217. New York (Academic Press). METZ, C. B., PITELKA, D. R., and WESTFALL, J. A., Biol. Bull. Wood's Hole, 104, 408. MUIR, A. R., i960. Quart. J. exp. Physiol., 45, 192. PITELKA, D. R., J. Protozool., 8, 75. ROBERTSON, J. D., Biochem. Soc. Symp., 16, 3. ROTH, L. E., J. biophys. biochem. Cytol., 2 (Suppl.), J. Ult. Res., 1, 223. SCHNEIDER, L., Z. Zellforsch., 50, 61. SEDAR, A. W., and PORTER, K. R., J. biophys. biochem. Cytol., 1, 583.
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