The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations

The epidermis of Xenoturbella bocki Westblad was studied by scanning and transmission electron microscopy. Two cell types predominate in the epidermis: multiciliated epidermal cells and non-ciliated or monociliated gland cells. A conspicuous feature is the dense ciliary coverage and the numerous gland cell openings. Xenoturbella has a characteristic pattern of axonemal filament termination in the distal tips of their cilia. Each epidermal cilium has the typical 9 + 2 patten through the major part of its shaft. Near the tip there is a shelf at which doublets 4–7 terminate. Doublets 1, 2, 3, 8 and 9 continue into the thinner distal part of the cilium. A similar shelf in cilia is known only from the turbellarian orders Nemertodermatida and Acoela, and hence may be an apomorphic feature which indicates a close relationship between Xenoturbellida, Nemertoder-matida and Acoela. The basal body is provided with a so-called basal foot which has a cross-striated appearance and an expanded distal plate that seems to act as a microtubule organizing center. Approximately 15–25 microtubuli radiate from the endplate of the basal foot to the basal bodies caudally. The arrangement of basal foot and ciliary rootlets in Xenoturbella differs from that of Acoela and related orders in that there are two striated rootlets only (an anterior and a posterior one), rather than one main rootlet and two lateral rootlets.     

Comparative ultrastructure of the epidermal ciliary rootlets and associated structures in species of the Nemertodermatida and Acoela (Plathelminthes)

 The fine morphology of epidermal ciliary structures in four species of the Nemertodermatida and four species of the Acoela was studied, with emphasis on Meara stichopi (Nemertodermatida). The cilium of M. stichopi has a distal shelf and is proximally separated from the basal body by a cup-shaped structure. The bottom of the cup consists of a bilayered dense plate, or basal plate. The basal body consists of peripheral microtubule doublets continuous with those of the cilium. In the upper part of the basal body, the doublets are set at an angle and are anchored to the enclosing cell membrane by Y-shaped structures. The lower part of the basal body tapers eventually. The striated main rootlet arises on the anterior face of the basal body, initially like a flattened strap, and continues along the basal body shaped as a tube which further down becomes solid. The hour-glass-shaped posterior rootlet arises on the posterior face of the basal body. Contrary to the main rootlet, the striations in the proximal part of the posterior rootlet run parallel to the microtubule doublets of the basal body. A pair of microtubule bundles lead from the posterior rootlet to the two main rootlets in the hind ciliary row, and follow these to their lower tip. In the other species of the Nemertodermatida studied, the structure of the ciliary basal body and the ciliary rootlets is similar to that of M. stichopi. Structural differences in the species of the Acoela are that the lowermost end of the basal body is narrow and bent forwards, the proximal part of the main rootlet is trough-shaped, the main rootlet is accompanied by a pair of lateral rootlets and the posterior rootlet with associated microtubule bundles is thin. The epidermal ciliary structures in species of the Nemertodermatida and Acoela have a number of shared characters which are unique within the Plathelminthes. However, almost all of these characters are found in Xenoturbella bocki (Xenoturbellida), and some even in species of other ”phyla” of the ”lower” Metazoa. Hence, these characters cannot be considered apomorphic for the Acoelomorpha. A character seemingly present only in species of the Nemertodermatida and Acoela is the bilayered dense plate. This feature might represent an autapomorphic character state for the Acoelomorpha. Accepted: 7 March 1997     

Fine structural observations on the ciliary receptors in the epidermis of three otoplanid species (Turbellaria proseriata).

In Notocaryoturbella bigermaria, Otoplana truncaspina and Paroto-planella heterorhabditica three types of epidermal receptors are recognized. Type I: with a single cilium running in a duct, piercing the distal dendrite process of the receptor. The internal wall of the dendrite process has eight ridges with longitudinal filaments lying inside them. The ciliary basal body lacks a longitudinal rootlet but is encircled by a thin annular formation. Type II: with a single (A) or several (B) cilia which protrude from the outer epithelial surface and are provided with a large and striped rootlet. Both types are considered as mechanoreceptors. Type III: with two or more short and stumpy cilia devoid of rootlets and displaying the usual 9 + 2 pattern in the proximal part only. They are considered as chemoreceptors.     

Comparative ultrastructure of the pharynx simplex in turbellaria

Summary The simple pharynges in thirteen species of Turbellaria in the orders Macrostomida, Haplopharyngida, Catenulida, and Acoela have been studied by electron microscopy. After consideration of the functional aspects of the pharynx simplex, the relationship of the pharynx simplex ultrastructure to the phylogeny of the above mentioned groups is analyzed.The Haplopharyngida and Macrostomida are united as a group by the following characters: a pharynx transition zone of 1–5 circles of insunk cells with modified ciliary rootlets or no cilia, pharynx sensory cells without stereocilia collars and with a variable number of cilia, a prominent nerve ring with more than 30 axons circling the pharynx at the level of the beginning of the pharynx proper distal to the gland ring, 2 or more gland cell types in the pharynx, with at least two layers of muscle present and the longitudinal muscles derived from regular and special body wall circular muscles and a prominent post-oral nerve commissure. This specific arrangement can be distinguished from the other pharynx simplex types and is called the pharynx simplex coronatus.The catenulid pharynx simplex is characterized by the lack of a prominent nerve ring, no prominent post-oral commissure, a transition zone with epidermal type ciliary rootlets, recessed monociliated sensory cells, and one or no type of pharynx gland cell. The Acoela are specialized because of the epidermal type rootlets in the pharynx proper. They also lack a transition zone and a prominent nerve ring and have monociliated sensory cells different from the catenulid type.Ultrastructural characters of the pharynx simplex support the view that the Haplopharyngida-Macrostomida are monophyletic. The more primitive catenulid pharynx probably arose from a common ancestral pool with the Haplopharyngida and Macrostomida, although it does not appear possible presently to establish a clear monophyletic line for these forms. The various pharynx types within the Acoela appear to indicate independent origins with no clear link to the basic pharynx simplex type in the three other orders.Abbreviations Used in Figures a nerve axon - ar accessory rootlet - bb basal body - bn brain-nerve ring commissure - c caudal rootlet - ce centriole - ci cilium - cm circular muscle - cp ciliary pit - cu cuticle - cw cell web - d dictyosome - dp proximal pharynx proper cell - e epidermis - er rough endoplasmic reticulum - f fibrous rod - g gastrodermis - gc gastrodermal gland cell - he heterochromatin - i intercellular matrix - lc lateral nerve cord - lm longitudinal muscle - m mitochondria - mo mouth - mt microtubules - mv microvilli - n nucleus - nr nerve ring - ns neurosecretory granules - p pharynx proper - ph pharynx - po post-oral commissure - r rostral rootlet - rm radial muscle - s sphincter - sc sensory cell - sj septate junction - sr sensory rootlet - t transition zone - u ultrarhabdite - v vertical rootlet - va food vacuole - za zonula adhaerens - 1 type I gland cell - 2 type II gland cell - 3 type III gland cell - 4 type IV gland cell - 5 type V gland cell - 6 type VI gland cell - 7 type VII gland cell     

Epidermal ciliary ultrastructure of adult and larval sipunculids (Sipunculida)

The ultrastructure of the ciliary apparatus of multiciliated epidermal cells in larval and adult sipunculids is described and the phylogenetic implications discussed. The pelagosphera of Apionsoma misakianum has a dense cover of epidermal cilia on the head region. The cilia have a long, narrow distal part and two long ciliary rootlets, one rostrally and one vertically orientated. The adult Phascolion strombus has cilia on the nuchal organ and on the oral side of the tentacles. These cilia have a narrow distal part as in the A. misakianum larva, but the ciliary rootlets have a different structure. The first rootlet on the anterior face of the basal body is very short and small. The second, vertically orientated rootlet is long and relatively thick. The two ciliary rootlets present in the larval A. misakianum are similar to the basal metazoan type of ciliary apparatus of epidermal multiciliated cells and thus likely represent the plesiomorphic state. The minute first rootlet in the adult P. strombus is viewed as a consequence of a secondary reduction. No possible synapomorphic character with the phylogenetically troublesome Xenoturbella was found.     

Ultrastructural study of the epidermis in two free-living Platyhelminthes, Mesostoma viaregginum and M. productum (Rhabdocoela, Typhloplanida)

Abstract. The epidermis of the free-living typhloplanids Mesostoma viaregginum and M. productum (Mesostominae) is described. In both species, the epidermis has polarized cells with nuclei located at the basal part of the cell, whereas mitochondria are in the apical one. The epidermis is entirely covered by microvilli and locomotory cilia anchored in the cytoplasm by vertical and horizontal rootlets. Rootlets exhibit distinct length and periodic structure in the two species. Furthermore, in each species vertical and horizontal rootlets possess different periodic structure. The pattern of termination of microtubules in epidermal cilia is described for the first time in the Typhloplanida; central microtubules shift along one axonemal side, doublets 1 and 6–9 lose their microtubule B, and gradually peripheral doublets become singlets. Finally, an electron-dense material caps the tip of the cilia. This pattern of termination closely resembles that of Temnocephalida, Kalytorhynchia, and Dalyelliida examined so far, but differences exist.     

Fine Structure of the Mastigont System in Tritrichomonas foetus (Riedmüller)*

SYNOPSIS. Tritrichomonas foetus shares many fine-structural features with the previously described genera of the subfamily Trichomonadinae. These include the arrangement and structure of the kinetosomes, of most rootlet filaments, including the sigmoid filaments of kinetosome #2, as well as those of the parabasal apparatus and of the pelta-axostyle complex. On the other hand, this species, and presumably all other Tritrichomonas augusta-type flagellates, differ from Trichomonadinae in certain important details. Among the features which T. foetus does not share with Trichomonadinae are the fine structure of the costa and of the undulating membrane, as well as several organelles not found in the latter subfamily. The costal base of Trichomonadinae is replaced in T. foetus and other Tritrichomonadinae by a comb-like structure, extending between the costa and the infrakinetosomal body. The suprakinetosomal body, connected to kinetosome #2 in the region of attachment of the sigmoid filaments, and the infrakinetosomal body, which appears to contribute to the proximal marginal lamella, are organelles evidently restricted to Tritrichomonadinae. The undulating membrane consists of 2 parts. The proximal part is a fold-like differentiation of the dorsal body surface, the dorsal part of which contains the proximal marginal lamella. The distal part of the undulating membrane, with no obvious physical connection to the fold, encloses the distal marginal lamella in its ventral, and the microtubules of the recurrent flagellum in its dorsal area. The organelle of T. foetus which by its size, certain structural characteristics, and relationship with the undulating membrane and some organelles, including the paracostal granules, is analogous to the costa of Trichomonadinae and of Trichomitopsis termopsidis (subfamily Tritrichomonadinae), conforms in the structure of its periodic cross-striations to that of the parabasal filaments of the latter organisms; its origin corresponds closely to that of parabasal filament 2 of Trichomonadinae.     

Ultrastructure of gill cilia and ciliary rootlets of Chaetoderma nitidulum Lovén 1844 (Mollusca, Chaetodermomorpha)

Cilia and associated structures on the gill lamellae on the ctenidum of Chaetoderma nitidulum were studied. The gill cilia are very long and have a whip-like narrow portion distally, where only three microtubule doublets continue to the distal tip. In the transition zone between the cilium and the centriolar triplet section of the basal body there is a dense plate, an aggregation of granules and a ciliary necklace with four strands. Further down there is a short cross-striated basal foot and two conical cross-striated ciliary rootlets. The first rootlet is flattened and directed forward. It connects distally with the basal feet of other adjacent cilia. The second rootlet is rounded in cross-section and vertically directed. The epithelial structures of Chaetoderma show similarities with other Mollusca. We found no structural characters that could support the current hypothesis of a close relationship of Xenoturbella to the Mollusca.     

Ciliary ultrastructure of protobranchs (Mollusca, Bivalvia)

Abstract. The external epithelial cilia and other surface structures of the nuculoid protobranchs Nuculana pernula and Nucula nitidosa were studied. The gill lamellae and labial palps are partly covered with very long cilia. These have a modified slender distal portion, an ordinary metazoan-type basal body, a basal foot. and a single, long cross-striated rootlet. In cilia on the gills of N. nitidosa , the basal foot is thick and attaches to the next basal body directly behind. Unciliated surface areas on the gills, labial palps, and foot are covered with a dense brushborder of microvilli. We observed no specific homologies between the cilia of the protobranchs studied and the epidermal cilia of the enigmatic Xenoturbella bocki , hence the recent hypothesis of a close connection of the latter to the protobranch bivalves is questioned.     

Fine Structure and Function of Pharynx Cilia in Glossobalanus minutus Kowalewsky (Enteropneusta)

Two kinds of cilia have been observed in the pharynx of Glossobalanus minutus Kowalewsky. From the present study, a ciliary specialization can be found in order to move a determinate substance, i.e. mucus or water. Mucus-moving cilia (type I cilia) have a single basal centriole and poorly developed ciliary rootlets. Their tips are rounded, bearing an inner, asymmetrical cap attached to some tubules. Water-moving cilia (type II cilia) are exclusively located at lateral epithelia of branchial bars, giving rise to the water current through the gills. They have two basal centrioles, proximal and distal, and a complex system of ciliary rootlets made up of a principal rootlet, a secondary or accessory rootlet and a 'fan' rootlet. The tips of type II cilia have a long process with some tubules inside. All basal structures are precisely orientated in order to assure a good coordination of ciliary beat. The possible functional significance of ciliary substructure is also discussed. From these observations a model for mucus and water currents through gill slits is postulated.     

Adaptation of a ciliary basal apparatus to cell shape changes in a contractile epithelium

Cilia projecting from the surfaces of highly contractile myoepithelia in the sea anemone Metridium senile maintain their basal orientation, and their ability to propel water, at different states of mesentery contraction, despite substantial changes of myoepithelial cell diameter and length. The ciliary basal apparatus in each monociliated myoepithelial cell is structurally well adapted to provide a stable anchorage for the cilium whilst compensating for these shape changes. It is composed of a distal centriole (basal body), a proximal centriole, a striated rootlet 2-3 micron long which is composed of a bundle of 4-6 nm filaments, and an arched rootlet, also striated, which is composed of a relatively loose bundle of 9-11 nm filaments. A single basal foot projects from the side of the distal centriole in the same direction as the path of the cilium during an effective-stroke; its tip is a focus for many microtubules that radiate outward in all directions toward the cell membrane. The arched rootlet forms a single arch in the cell apex, also in the same plane as the path of the cilium during an effective-stroke. The central axis of the basal apparatus, that is through the distal centriole and the striated rootlet, passes through the apex of the arch. The arched rootlet is apparently flexible so that it can increase or decrease its span as the cell increases or decreases in diameter. In pharnyx and siphonoglyph cells from M. senile, which do not undergo great changes in diameter or length, there is no arched rootlet, and the striated rootlet is much longer. The broad structural diversity of the metazoan ciliary basal apparatus must to a large extent be related to the diversity of the structural and mechanical properties of the cells in which it occurs.     

The ventral epithelium of Trichoplax adhaerens (Placozoa): Cytoskeletal structures,cell contacts and endocytosis

Summary All cilia emerge from ciliary pits supported along their circumference by 22–24 dense rodlets that are connected by filaments to a surrounding sheath of endoplasmic reticulum. The proximal part of the basal body is provided with two short lateral rootlets and one long terminal rootlet, all associated with microtubules. The lateral rootlets are in turn connected by fine fibrous material to the dense supporting rodlets which follow the contour of the ciliary pit and extend along the ciliary membrane beyond the level of the basal plate where the central pair of microtubules originates. The proximal part of the basal body has fine fibrous connections to the endoplasmic reticulum while its distal portion is surrounded by nine curved sheets. The terminal cell contactions are by belt desmosomes that are accompanied by a bundle of microfilaments which encircle the apical region of the cell and insert at the cell membrane. Tight junctions are lacking. Endocytosis was demonstrated by the uptake of cationized ferritin. The structures associated with the ciliary pits are probably associated with the firm anchorage of the ciliary base since Trichoplax adheres to the substrate as it moves propelled by its ventral cilia. The marginal bundle of microfilaments may be involved in folding of the organism during feeding.     

The ciliary rootlet maintains long-term stability of sensory cilia

The striated ciliary rootlet is a prominent cytoskeleton originating from basal bodies of ciliated cells. Although a familiar structure in cell biology, its function has remained unresolved. In this study, we carried out targeted disruption in mice of the gene for rootletin, a component of the rootlet. In the mutant, ciliated cells are devoid of rootlets. Phototransduction and ciliary beating in sensory and motile cilia initially exhibit no apparent functional deficits. However, photoreceptors degenerate over time, and mutant lungs appear prone to pathological changes consistent with insufficient mucociliary clearance. Further analyses revealed a striking fragility at the ciliary base in photoreceptors lacking rootlets. In vitro assays suggest that the rootlet is among the least dynamic of all cytoskeletons and interacts with actin filaments. Thus, a primary function of the rootlet is to provide structural support for the cilium. Inasmuch as photoreceptors elaborate an exceptionally enlarged sensory cilium, they are especially dependent on the rootlet for structural integrity and long-term survival.     

CFAP53 regulates mammalian cilia-type motility patterns through differential localization and recruitment of axonemal dynein components

Motile cilia can beat with distinct patterns, but how motility variations are regulated remain obscure. Here, we have studied the role of the coiled-coil protein CFAP53 in the motility of different cilia-types in the mouse. While node (9+0) cilia of Cfap53 mutants were immotile, tracheal and ependymal (9+2) cilia retained motility, albeit with an altered beat pattern. In node cilia, CFAP53 mainly localized at the base (centriolar satellites), whereas it was also present along the entire axoneme in tracheal cilia. CFAP53 associated tightly with microtubules and interacted with axonemal dyneins and TTC25, a dynein docking complex component. TTC25 and outer dynein arms (ODAs) were lost from node cilia, but were largely maintained in tracheal cilia of Cfap53^-/- mice. Thus, CFAP53 at the base of node cilia facilitates axonemal transport of TTC25 and dyneins, while axonemal CFAP53 in 9+2 cilia stabilizes dynein binding to microtubules. Our study establishes how differential localization and function of CFAP53 contributes to the unique motion patterns of two important mammalian cilia-types.     

Epidermal ultrastructure of the adult parasitic phase female and encapsulated larva of Kronborgia isopodicola (Platyhelminthes, Fecampiidae): Phylogenetic implications

The parasitic phase female K. isopodicola possesses a ciliated epidermis of polyhedral cells. Adjacent lateral plasma membranes are separated at intervals creating intercellular spaces. Epidermal cilia are anchored by a horizontal rootlet, opposite which a spur projects from the basal body, and a narrow vertical rootlet. The cytoplasm contains coated vesicles, and coated pits lie between microvilli. Large granular and vesicular bodies (rhabdoids) are scattered through the epidermal epithelium; in the epidermis of the encapsulated larva, granular rhabdoids are densely packed and slender, more compact bodies also occur. The compact, granular and vesicular bodies are probably morphological variants of the same epidermal structures, suggested to undergo sequential changes accomplished in later stages by lysosomal activity. Morphologically similar epidermal bodies are found in triclads. They are also characteristic of the parasitic genus Urastoma, which shares other ultrastructural features with K. isopodicola. The Neodermata may have arisen from parasitic turbellarian forms, at a more “primitive” level of organization than ancestors of the contemporary Rhabdocoela.     

The Mastigont System of Trichomonas gallinae (Rivolta) as Revealed by Electron Microscopy

SYNOPSIS. The fine structure of Trichomonas gallinae has been examined by electron microscopy and correlated with previous light microscope observations. A composite diagram of the flagellate, derived from both types of examination, is presented. Details of relationships of various mastigont organelles are documented by electron micrographs. The extent of the pelta and its connection to the capitulum of the axostyle have been determined. Four types of kinetosome rootlets have been described. One consists of superficial “filaments” radiating from each of the 9 triplet microtubules of kinetosomes #1, #2 and #3. A 2nd type of rootlet structure is represented by single comma-shaped filaments emerging clockwise from kinetosomes #1 and #3. The filament from kinetosome #1 has a periodic structure similar to that of the marginal lamella with which it is believed to connect. A 3rd type of rootlet emerges from kinetosome #2 as a sheet of about 9 filaments which traverse a sigmoid course and terminate on the inner surface of the microtubules of the pelta near the peltar-axostylar junction. The 4th set of structures consists of the costa and parabasal filaments. These structures have major periodicities of similar dimension but have readily differentiable repeating units. The costa appears to originate at the kinetosome of the recurrent flagellum, but its origin is also contiguous with that of parabasal filament 2 which has some continuity with kinetosomes #2 and #3. Parabasal filament 1, on the other hand, arises solely from or near kinetosome #2. Occasional observations of a costa and a parabasal filament in juxtaposition over a great part of their length has led to the suggestion that the parabasal filament may play a role in the development of the costa. Periodic and filamentous structures have been observed in paraxostylar and paracostal granules and in nearby cytoplasm. Their possible role in providing substance for the developing axostyle and the costa is discussed. The results are discussed in the light of available information pertaining to structure of various trichomonad species as revealed by light and electron microscopy.     

Ultrastructural evidence for the occurrence of three types of mechanosensitive cells in the tentacles of the cubozoan polypCarybdea marsupialis

Summary The ectodermal cell layer in the tentacles of the cubozoan polypCarybdea marsupialis contains four types of cells (types 1–4) bearing specialized cilia. Epitheliomuscular cells (type 1) are characterized by motile cilia with dynein-decorated axonemes. 200 nm long extramembranous filaments of unknown function are restricted to a belt-like region distal to the transition zone. Up to 40 rn long rigid cilia formed by a slender epithelial cell type (type 2) are surrounded by rings of short microvilli. The axonemes of these cilia are composed of incomplete microtubules and lack dynein. Microvilli and cilia are linked by intermembrane connectors. Microtubuledoublets and ciliary membrane are interconnected by microtubule-associated cross-bridges only within this contact region. At the tip of each tentacle a single nematocyte (type 3) is surrounded by 7–10 accessory cells (type 4). These both cell types are equipped with similar cilium-stereovilli-complexes consisting of a cone-like arrangement of stereovilli and a modified cilium. The axonemal modifications of the cilium, its interconnections with the surrounding stereovilli and the linkages between ciliary axoneme and ciliary membrane are similar to those known from the cnidocil-complexes of hydrozoons and other epithelial mechanosensitive cells of the collar-receptor type. Our data indicate that besides the nematocyte two other types of mechanosensory cells (types 2 and 4) are integrated in the ectodermal cell layer ofCarybdea which possibly affect the triggering mechanism of nematocyst discharge.