Ultrastructure of epidermal eyespots of Microstomum lineare (Turbellaria, macrostomida)

Cell Tissue Res. 210, 21-32 (1980) Cell and Tissue Research �9 by Springer-Verlag 1980

Ultrastructure of Epidermal Eyespots of Microstomum lineare (Turbellaria, Macrostomida)

Irmeli Palmberg, Maria Reuter, and Marianne Wikgren

Institute of Biology, Abo Akademi, Finland

Summary. The eyespots of M i c r o s t o m u m lineare were studied by electron microscopy, light microscopy, and fluorescence microscopy. Each eyespot consists of two ciliary photoreceptor cells shielded by pigment cells and additional sensory cells. The photoreceptor cells are characterized by a distal intracellular cavity lined with 50-100 interwoven cilia. The other sensory cells are of two ultrastructurally different types, one with long cilia predominating and the other with balloonlike cilia. The pigment cells, which envelop processes of the sensory cells, contain pigment vacuoles varying in size and content and give a bright red fluorescence by the Falck-Hillarp method. The eyespots are suggested to perform a dual function as photoreceptors and chemoreceptors. The evolutionary significance of ciliary photoreceptors in Turbellaria is discussed.

Key words: Eyespots - Photoreceptor - Chemoreceptor - Turbellaria - Ultrastructure.

The eyes of most Turbellaria are of the typical pigment-cup type, lying deep in the mesenchyme above or within the brain. With the exception o f M i c r o s t o m u m lineare epidermal pigmented eyes or eyespots are very rare (Hyman 1951). The fine structure of photoreceptors of polyclads (MacRae 1966), triclads (R6hlich and T6r6k 1961; Carpenter et al. 1974, MacRae 1964), proseriates (Bedini and Lanfranchi 1974) and neorhabdocoels (Bedini et al. 1973) have been classified as "rhabdomeric" (see Eakin 1972). In addition to rhabdomeric pigment-cup eyes, some turbellarians have pericerebrally located ciliary aggregations (Ehlers and Ehlers 1977b) or a ciliary lamellate body (Ehlers and Ehlers 1977a) with presumed photoreceptive function.

The present investigation deals with the fine structure of the epidermal pigmented eyespots of a macrostomid turbellarian, Micros tomum lineare, and

Send offprint requests to: I. Palmberg, Institute of Biology, Abo Akademi, 20500 Abo 50, Finland

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22 I. Palmberg et al.

compares its ultrastructure with that of known photoreceptors of other invertebrates. The significance of ciliary photoreceptor cells in turbellarians and the probable dual function of the eyespot areas as photoreceptors and chemoreceptors are discussed.

Materials and Methods

Specimens of Microstomum lineare (MiJller 1774) (order Macrostomida) were caught in shallow brackish water at Stortervo, Pargas, and in freshwater at Teijo, Bj~irn~t (SW Finland) during the summers of 1978 and 1979. They were fixed in 2.5 % glutaraldehyde buffered with 0.2 M collidine buffer, pH 7.4, at 4 ~ C for one hour, washed three times in the same buffer for about one hour, postfixed for one hour in cold collidine-buffered 1% OSO4, and embedded in Epon 812 (Luft 1961). Ultrathin sections cut transversely, sagittally, and longitudinally were mounted on Formvar-coated copper grids, stained with uranyl acetate and lead citrate, and examined with a U EMV-100 V (USSR) electron microscope. For light microscopy 0.95 I~m Epon sections stained with methylene blue azure lI basic fuchsin (Humphrey and Pittman 1974) or with methyl green - pyronine (Jurand and Goel 1976, slightly modified) were examined with a Leitz Ortholux microscope. For fluorescence microscopy whole worms were frozen, freeze-dried, and treated with formaldehyde gas in accordance with the specific method for the cellular demonstration of biogenic monoamines described by Falck and Hillarp (Bj6rklund et al. 1972).

Fig. 1. Diagram of eyespot of Microstomum lineare. B brain; BC balloonlike cilium; E epidermis; LC long cilium; M muscle; N F nerve fibre; PC pigment cell; RC photoreceptor cell; SC other sensory cell

Fig. 2. Electron micrograph of section through photoreceptor process showing central lumen with numerous interwoven cilia (c). Note mitochondria (m/), neurotubuli (nt), vacuoles (v) and dense-core vesicles (dcv) in surrounding cytoplasm. Arrows indicate small droplike vesicles in cilia. • 19,000

Fig. 3. Photoreceptor process showing basal bodies (bb) giving rise to cilia with proximal ring of 9 pairs of tubules ending in two single tubules. Note coated vesicles (cv) pinching off from cilia (arrow); rni mitochondria; nt neurotubuli; v vacuoles; dcv dense-core vesicles. • 19,000


Results

M i c r o s t o m u m lineare possesses a pair of eyespots, situated dorsally at the anterior end of the body. They are of the epidermal pigment-spot type (Hyman 1951). In the living animal the eyespot areas appear as red to yellow streaks, giving a bright red fluorescence by the Falck-Hillarp method. Both light and fluorescence microscopy reveal nerve fibres leading from the eyespot areas to the brain. The epithelium overlying the eyespots appears modified, bearing tightly packed microvilli and slender cilia. The eyespots average 1701xm in length, 30~tm in ventrodorsal diameter and 40 ~tm in mediolateral diameter.

Ultrastructural studies show several different cell types. Anterolaterally to the brain, phororeceptor cells with ciliary processes lie immediately beneath the subepidermal muscle layer. In addition, large pigment cells envelop processes of sensory cells of two types, some having long cilia and others balloonlike cilia (Fig. 1).

Photorecep tor Cells

Photoreceptor cells consist of a cell body bearing a distal process that does not perforate the epithelium. In the walls of a central, ovoid lumen (4-7 ~tm in diameter), 50-100 basal bodies are embedded (Fig. 2), each with the typical centriolar pattern of nine triplets ofmicrotubules (Fig. 3). The basal bodies give rise to a corresponding number of cilia projecting into the lumen. The pattern of nine internal, paired tubules is soon lost as the cilium flattens out distally, but its tip has at least two single microtubules (Figs. 2, 3). There are no ciliary rootlets.

The cell body of these photoreceptor cells lies deep in the mesenchyme. The more or less circular nucleus is about 10 Ixm in diameter and has finely dispersed chromatin. The cytoplasm contains a well developed Golgi complex, lamellar bodies and dense-core vesicles, as well as several coated vesicles (Fig. 3). Near the nuclear envelope a few usually long mitochondria contain several cristae parallel to their long axes. Numerous mitochondria, however, appear at the rim of the cytoplasm lining the central lumen. The peripheral cytoplasm contains a few cisternae of granular endoplasmic reticulum and also vacuoles of various sizes, neurotubules, and a few scattered ribosomes. Small droplike vesicles are found between the ciliary membranes in the process (Fig. 2). Nerve fibres containing dense-core vesicles are associated with the photoreceptor cells, but no synaptic areas have been observed.

Fig. 4. a Sensory cell processes (sp) invaginating pigment cells (PC), connected with surrounding cells by septate desmosomes (sd). mi mitochondria; nt neurotubuli; v vacuole, x 12,000. b Longitudinal section through sensory cell process (sp) with long cilia, showing electron-lucent loop (l) of modified distal tip of cilium. • 12,000

Fig. 5. Longitudinal section through sensory cell process showing finely granular centre (arrow) in basal part of cilium, several dense-core vesicles (dcv) and neurotubuli (nt); bb basal body. • 38,000

Fig. 6. a Transverse section through basal part of cilium of sensory cell with long cilia, showing 9 double tubules and granular centre (arrow). • 38,000. b Paired tubules changing apically into single tubules. • 60,000

Eyespots of Microstomum lineare 25


Fig. 7. Transverse section through cilia (BC) of sensory cell with balloonlike cilia and longitudinal section of sensory cell process with long cilia (LC). Note ring of 9 double tubules (arrows), and difference in diameter between BC and LC; nt neurotubuli; pv pigment vacuole; sd septate desmosome. • 25,000

Fig. 8. Longitudinal section of balloonlike cilium, showing basal body (bb) with basal plate (bp) and diverging tubules (t) in fine fibrillar matrix (ma). x 45,000

Additional Sensory Cells

The processes o f the other sensory cells are connected with the surrounding epithelium, with each other, and with the enveloping pigment cells by means o f septate desmosomes (Figs. 4a, 7). The cytoplasm has a low electron density. Numerous neurotubules in the cellular processes run parallel to their long axes. Several elongated mi tochondr ia with irregular cristae are located in the sensory cells between and parallel to the neurotubules. In addition, the cytoplasm contains dense-core vesicles and vacuoles o f different sizes (Figs. 4a, b, 5). The cell bodies o f the sensory cells lie in the cortical layer o f the cerebral ganglion.

The Sensory Cell With Long Cilia is the dominan t type in the posterior par t o f the eyespot. It bears three long, divergent cilia and several slender microvilli


Fig. 9. Eyespot, showing pigment cells (PC) with pigment vacuoles (pv); vacuoles composed of small granules (pv) in basal parts of cell, apically of amorphous material (pv). SC sensory cell. x 12,000

Fig. 10. Part of pigment cell showing internal structure of pigment vacuole (pv). x 30,000. a Lamellar structure (arrow) inside pigment vacuole, b Numerous small granules (arrow) inside pigment vacuole

(Figs. 4a , b). The cil ia rest on a basa l b o d y wi thou t a root le t . Ins tead o f the pa i r o f centra l mic ro tubu les charac ter i s t ic o f mot i le cilia, each ci l ium conta ins in its basa l pa r t a finely granular , cone-shaped centre (Figs. 5, 6 a). The pa t t e rn o f nine double t s o f mic ro tubu les is lost in the more apical par t s o f the c i l ium (Fig. 6 b). Occas iona l ly the dis ta l t ip appea r s modif ied , an axoneme fo rming a c i rcular l oop o f low elect ron


density (Fig. 4b). This must be regarded as a fixation artefact, as is the paddle cilium in some marine turbellarians reported by Ehlers and Ehlers (1978).

The Sensory Cell With Balloonlike Cilia differs from that with long cilia only in the structure of the cilia. This cell has three short (1-2 I~m), balloonshaped cilia. The finely granular material observed in the long cilia is lacking here. The basal body, devoid of a rootlet, is characterized by a basal plate and continues, as nine double tubules, into the basal part of the axoneme (Fig. 7). In longitudinal section, however, the tubules become single towards the apex. The matrix of each cilium is of fibrous material (Figs. 7, 8). The difference in diameter between the balloonlike cilium and the long cilium may be as much as 1.2 ~tm.

Pigment Cells

The pigment cells, which are deeply invaginated by the sensory cells, contain a special product (Fig. 9). When treated by the Falck-Hillarp method, this material emits a bright red fluorescence. The round and membrane-bounded pigment granules, up to 2 ~tm in diameter, contain a mass of smaller, round (30-100 nm in diameter) granules (Fig. 10b). The pigment vacuoles lie in the vicinity of the Golgi complex. They appear to originate by coalescence of smaller granules that budd off from the Golgi apparatus. Apically, towards the microvillus-bearing surface, they lose their granular contents and harbor only a light amorphous material (Fig. 9). Lametlar structures surrounded by amorphous material may occasionally occur inside of vacuoles (Fig. 10a).

Several microtubules extend longitudinally in the cytoplasm. The cell body lies immediately beneath the muscle layer. The globular nucleus, surrounded by an irregularly dilated nuclear envelope, appears finely granular and contains several dense condensations of chromatin material and a prominent nucleolus. A sparse endoplasmic reticulum lies peripheral to the nucleus. Scattered, free ribosomes and vacuoles of various sizes are also present in the electron dense cytoplasm. Mitochondria with irregular cristae are concentrated near the nuclear envelope and in the apical parts of the pigment cell (Fig. 9).

Discussion

Photoreceptor Cells. The most likely photoreceptors in positively phototactic Microstomum lineare are of the ciliary type. The ciliary membranes, however, are not expanded into discs or villi, such as those characteristic of most animal photoreceptors. There is increasing evidence that a cilium may acquire light sensitivity without any morphological modifications (Brandenburger et al. 1973). Primitive photoreceptors may consist simply of a bundle of cilia (Woollacott and Eakin 1973) or a ciliary aggregation (Ehlers and Ehlers 1977b).

Although there is as yet no physiological evidence that the cells described in the eyespots are light-sensitive, this role is indicated by several morphological similarities with known and presumed invertebrate photoreceptors. They have


many elongated mitochondria close to the ciliary lumen. The ciliary microtubule pattern is 9 + 0 typical of photoreceptors. The cellular process contains dense-core vesicles similar to those described in photoreceptors by Eakin and Westfall (1965). In the rhabdomeric eyes the coated vesicles, present also along the whole length of the receptor process in Microstomum, are supposed to have important functions in membrane transport to or from the microvilli (R6hlich 1977). The droplike vesicles around the ciliary lumen may also have a membrane transport function. The cytoplasmic vesiculation, described in the present material, is supposed to be involved in the breakdown of visual products or in the transport of photosensitive substances, neurotransmitters, and other materials (MacRae 1966; Bedini et al. 1973). This hypothesis was supported by Brandenburger and Eakin (1970) who, in a snail eye, followed the cytoplasmic route of the photopigment with isotope-labelled vitamin A from the Golgi complex through photic vesicles into the microvilli.

Additional Sensory Cells. Receptors with features similar to the two types described are present in organisms belonging to different systematic groups. In monogeneans, Lyons (1973) described multiciliate receptors with a presumed chemoreceptive function in ciliated pits, morphologically similar to the receptors with long cilia of Mierostomum. Further similarities exist with the multiciliated receptors of type III present in some turbellarians, which are considered to be chemoreceptors (Bedini et al. 1975), and with the sensory cells in the eyespot of a nematode (Burr and Burr 1975).

Receptors with balloonlike cilia have been described in a few turbellarians (Schockaert and Bedini 1977), but in contrast to those of Microstomum several of them have a rudimentary rootlet (Koie and Bresciani 1973; Reuter 1975). Analogous structures have been reported in the pineal organ of vertebrates (Oksche and Kirschenstein 1969).

So far, all conclusions regarding the functions of the various receptors have to be based on analogies, and a distinction between chemoreceptors and mechano- receptors on purely morphological grounds is as yet impossible. The similar morphology of the amphid of a nematode described by Burr and Burr (1975), however, suggests a probable chemoreceptive function for the eyespot area. Moreover, a number of structural details typical of vertebrate and invertebrate olfactory receptors are observed in the sensory cells of the eyespot of Microstomum. Despite contact with the external environment the sensory cilia are modified to have a distinct proximal segment, decreasing distally in diameter. This feature and the disruption of the patterned doublet into random singlets are characteristics of vertebrate olfactory cilia, as is the absence of basal feet and a rootlet (Burr and Burr 1975). The sensory cell processes are enveloped by pigment cells, as in the nematode amphid.

Pigment Cells. The enveloping pigment cells probably serve the sensory cells metabolically, for they contain numerous large vacuoles. The contents of these vacuoles range from relatively homogeneous to clearly lamellar in structure. This difference may be related to the stage in the formation of pigment (Carpenter et al. 1974) or to effects of tissue preparation (Brandenburger et al. 1973). Lamellar structures have also been observed in the pigment granules of planarian eyes


(R6hlich and T6r6k 1961). According to Needham (1974), integumental pigment granules develop in the endoplasmic-reticulum-Golgi systems, whereby the matrix filaments aggregate into sheets which appear to become wound concentrically. These observations support the hypothesis that the pigment granules exist in different physiological states. The chemical nature of the pigment is unknown, but the red pigment in living animals displays a bright red fluorescence with the Falck- Hillarp method. This suggests the presence of either carotenoids or porphyrins (Fox and Vevers 1960). Both of these widespread pigment classes have been observed in connection with invertebrate photoperception (Wolken and Mogus 1979). For chemoreception, most of the evidence seems to be in favour of carotenoids (for review, see Needham 1974). Furthermore, biochromes in fluid vacuoles usually prove to be free carotenoids in a lipid medium (Fox 1953).

Evolutionary Aspects

The fine structure of the eyespots of the turbellarian M. lineare does not support Eakin's hypothesis (1972) that the platyhelminthes are members of the rhabdomeric, rather than the ciliary, line of evolution of photoreceptors. The division into ciliary and rhabdomeric evolutionary lines is not complete (Barber and Wright 1969). Flatworms may possess both receptor types, although in separate eyes. Thus, besides the predominating rhabdomeric eyes, ciliary aggregations or lamellate bodies with presumed photoreceptive function are reported in larval Monogenea and Digenea, as well as in the oncomiracidium of Entobdella (Lyons 1973), in miracidia and cercariae of Fasciola and Schistosoma (Wilson 1970; Brooker 1972), and in some turbellarians (Ehlers and Ehlers 1977a, b). Other exceptions to the general grouping of invertebrate photoreceptors are eyes containing both types of receptor, as in some molluscs (Barber et al. 1967; Boyle 1969), or eyes possessing both ciliary and rhabdomeric elements in the same photoreceptor, as in tornarian larvae (Brandenburger et al. 1973). Also, more or less reduced cilia or ciliary formations can be found in rhabdomeric photoreceptors (Clark 1967; Eakin et al. 1967). These findings, together with Ruppert's observation of ciliary eyes in turbellarian larvae (1978), support the hypothesis put forward by Vanfleteren and Coomans (1976) that the differences among photoreceptor types is more quantitative than qualitative, varying from predominantly ciliary to predominantly rhabdomeric.

Functional Significance

The presence of two photoreceptor types in the same organism supports the view of differences in function. Thus, cilium-type receptors may have a greater sensitivity to low levels of illumination than rhabdomeric eyes, as suggested by Brooker (1972). Barber and Wright (1969) demonstrated electrophysiologically that the ciliary eyes in the mollusc Cardium produce "off' responses to light and mediate a protective shadow response, while rhabdomeric eyes produce "on" response to light. The same function, i.e., signalling the presence of shadows, was suggested by Lyons (1973) for

Eyespots of Microstomurn lineare 31

ciliary eyes of the monogenean Entobdella, in contrast to that of pigmented rhabdomeric eyes. Alternatively they might be involved as long-term light receptors setting some diurnal or nocturnal activity phase, or the time of hatching (Kearn 1978). The habit of living in deep or shallow waters might even be a modification factor (Ehlers and Ehlers 1977b). There are, however, insufficient data to support this "off' and "on" generalization, and exceptions do occur.

The eyespots of M. lineare are particularly interesting as they may have a dual function as photoreceptors and chemoreceptors. On purely morphological grounds it can be presumed that the pigment cells enveloping the sensory cells assist an olfactory structure and shade the neighbouring photoreceptors, enabling a transparent organism to detect the direction of a light source relative to body orientation. A similar dual function has been ascribed to the amphids of some nematodes (Burr and Burr 1975). Further electrophysiological studies will have to provide more data on the light-sensitive and putative olfactory organelles of Microstomum, as will autoradiographic analyses of the presumed photopigment in the pigment cells.

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Accepted April 22, 1980

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Ultrastructure of epidermal eyespots of Microstomum lineare (Turbellaria, macrostomida)