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The alveolocysts of the Nassulida: Ultrastructure and some phylogenetic considerations

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... For example, the transfer of Synhymeniida to Phyllopharyngea was supported by ultrastructural features of the pellicle and kinetosome (Kivimaki et al. 1997;Small and Lynn 1985). Within Nassophorea, the features of Microthoracida, such as the absence of the cartwheel in the kinetosomes and the longitudinal rows of cilia intramembrane particles are all different from Nassulida (Bardele 1981;Eisler 1988;Eisler and Bardele 1983). Therefore, the combination of ultrastructure and molecular information may provide a more objective solution to the systematics problem of Nassophorea. ...
... To date, the detailed ultrastructural studies on Nassophorea are limited and are mainly concentrated in several genera. They are Furgasonia, Nassula, Leptopharynx, and Pseudomicrothorax, and the former two belong in the order Nassulida, whereas the latter two belong in the order Microthoracida (de Puytorac and Njiné 1980;Eisler 1988;Eisler and Bardele 1983;Njiné and Didier 1980;Peck 1977). Discotricha papillifera, representing the order Discotrichida, was reported only with brief ultrastructural images of the cortex in the oral region (Wicklow and Borror 1977). ...
... The alveoli of Furgasonia and Nassula usually have septa located between two alveolocysts of a pair and are distributed randomly in the alveolar space. Instead, in Pseudomicrothorax, the alveolus shows a continuous flat space that surrounds the entire cell and finds no alveolar septa (Eisler 1988;Eisler and Bardele 1983;Peck 1977). In Apocolpodidium, the existence of septa is similar to that in Furgasonia and Nassula. ...
Article
The Class Nassophorea is not monophyletic with unsolved relationship of four orders, which calls for discussion to combine morphological features and molecular phylogeny. In the present study, the ultrastructure of Apocolpodidium etoschense in the order Colpodidiida is first studied. Comparisons between orders of Nassophorea were conducted and a discussion of systematics was performed based on a SSU rRNA gene-based phylogeny. The order Colpodidiida and Nassulida shared the following features: Two pairs of alveolocysts in the cortex, the presence of a ‘‘B-cartwheel’’ in the proximal region of the kinetosome, the presence of cytostomal lamellae and subcytostomal lamellae in the cytopharyngeal basket, and spindle trichocysts with a simple tip. These similarities shape a core group of Nassophorea, which are morphologically and genetically different from the order Microthoracida. Consequently, Microthoracida should be regarded as an independent taxon rather than a member of Nassophorea. Within the core group of Nassophorea, Colpodidiida as an independent order is further validated by its delicate cytopharyngeal basket which lacks nematodesmal lamellae; while the non-monophyly of the order Nassulida might be explained by differentiation of the cartwheels in kinetosomes and the arrangement of kinetosomes with postciliary microtubules in the nassulid organelle within its members.
... Alveolocysts and intraordinal classification. Alveolocysts are a special cortex pattern as yet found in Furgasonia blochmanni, Nassula aurea, N. citrea, N. ornata, N. tumida, and Pseudomicrothorax dubius (Eisler & Bardele 1983). Based on , who classified Pseudomicrothorax and Leptopharynx in the same family, Leptopharyngidae Kahl, 1926;Eisler and Bardele (1983), , and Gong et al. (2009) obviously assumed that Leptopharynx has alveolocysts. ...
... Alveolocysts are a special cortex pattern as yet found in Furgasonia blochmanni, Nassula aurea, N. citrea, N. ornata, N. tumida, and Pseudomicrothorax dubius (Eisler & Bardele 1983). Based on , who classified Pseudomicrothorax and Leptopharynx in the same family, Leptopharyngidae Kahl, 1926;Eisler and Bardele (1983), , and Gong et al. (2009) obviously assumed that Leptopharynx has alveolocysts. However, they did not know the study by Njine´and Didier (1980), who showed by transmission electron microscopy the absence of alveolocysts in Leptopharynx. ...
... Ciliates are characterized by a complex cortex composed of the plasma membrane, membrane-bounded alveoli, rows of basal bodies with associated microtubular and fibrillar structures, and a membrane skeleton called the epiplasm. In Pseudomicrothorax dubius, the epiplasm is a very prominent layer of about 150 nm thickness, and it has been the subject of several ultrastructural studies (Eisler and Bardele, 1983;Faure-Fremiet and Andre, 1967;Hausmann, 1979;Hausmann and Mulisch, 1981;Peck, 1977). Among the functions ascribed to it are those of cell shape maintenance and the structural integration of the diverse cortical elements such as the ciliary basal bodies (Grain, 1986;Hausmann and Mulisch, 1981;Peck, 1977). ...
Article
The membrane skeleton, or epiplasm, is part of the structurally complex ciliate cortex. It is thought to have skeletal functions concerning the spatial organization of cortical elements such as the basal bodies. Here we report the biochemical and immunological characterization of some components of the purified epiplasm of Pseudomicrothorax dubius. The epiplasm proteins consist of two quantitatively major groups of proteins, one of 76–80x103Mr, the other of 11–13x103Mr, which appear to be the principal structural elements of the epiplasm, and a series of minor components of 62–18x103Mr. Based upon lectin labeling and glycosidase treatment, some of the latter have been identified as glycoproteins. Using affinity-purified antibodies specific for individual glycoproteins or groups of glycoproteins, we were able to localize them in situ by immunoelectron microscopical methods. This in situ localization demonstrates that the glycosylated epitopes, unlike the glycoresidues of membrane proteins, are distributed throughout the entire epiplasmic layer rather than being restricted to regions adjacent to the cortical membranes. Thus, these proteins represent glycosylated, cytoskeletal elements. At least one of these glycoproteins (Mr 62x103) shows positive immunoreactivity with a monoclonal antibody (Pruss anti-IFA) recognizing most intermediate filament (IF) proteins, indicating that IF proteins might be present in protozoan cytoskeletons.
... The systematic position of synhymenians has long puzzled taxonomists, and their assignment to the class Nassophorea (nassulids and microthoracids) or to the Subkinetalia have been controversial. Synhymenians share ultrastructural and morphological similarities with both Nassophorea and Phyllopharyngea, suggesting that they are likely a transition group between these two classes (Eisler and Bardele, 1983;Small and Lynn, 1985;Kivimaki et al., 1997;Lynn and Small, 2002). A comprehensive comparison of morphology and ultrastructure among synhymenians, Nassophorea, and the Subkinetalia has previously addressed this issue (Gong et al., 2009). ...
Article
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Ciliated protists (ciliates) are widely used for investigating evolution, mostly due to their successful radiation after their early evolutionary branching. In this study, we employed high-throughput sequencing technology to reveal the phylogenetic position of Synhymenia, as well as two classes Nassophorea and Phyllopharyngea, which have been a long-standing puzzle in the field of ciliate systematics and evolution. We obtained genomic and transcriptomic data from single cells of one synhymenian (Chilodontopsis depressa) and six other species of phyllopharyngeans (Chilodochona sp., Dysteria derouxi, Hartmannula sinica, Trithigmostoma cucullulus, Trochilia petrani, and Trochilia sp.). Phylogenomic analysis based on 157 orthologous genes comprising 173,835 amino acid residues revealed the affiliation of C. depressa within the class Phyllopharyngea, and the monophyly of Nassophorea, which strongly support the assignment of Synhymenia as a subclass within the class Phyllopharyngea. Comparative genomic analyses further revealed that C. depressa shares more orthologous genes with the class Nassophorea than with Phyllopharyngea, and the stop codon usage in C. depressa resembles that of Phyllopharyngea. Functional enrichment analysis demonstrated that biological pathways in C. depressa are more similar to Phyllopharyngea than Nassophorea. These results suggest that genomic and transcriptomic data can be used to provide insights into the evolutionary relationships within the “Nassophorea–Synhymenia–Phyllopharyngea” assemblage.
Article
The class Nassophorea includes the microthoracids and nassulids, which share morphological similarities in their somatic kinetids and cytopharyngeal baskets. The monophyly of this clade has been challenged by small subunit rRNA gene sequences and multi-gene analyses that do not provide strong support. To provide a more robust test of the monophyly of the Nassophorea, phylogenomic analyses were based on 124 genes derived from the single-cell transcriptomes of the microthoracid Pseudomicrothorax dubius and the nassulid Furgasonia blochmanni. The nassulid Nassula sorex from the Culture Centre for Algae and Protozoa was also included, but this isolate was discovered to have been misidentified. We first redescribe, using light and scanning electron microscopical techniques, this “N. sorex” as a new species of Nassula, Nassula variabilis n. sp., characterized by its highly variable nassulid frange. We have sequenced the single-cell transcriptomes to obtain data for phylogenomic analyses. These gave robust support for the Nassophorea, which are sister to a clade of Colpodea species. If our topology truly represents the order of divergence of taxa, a cytopharyngeal basket with microtubular nematodesmata and with Y and Z microtubular ribbons was likely an ancestral feature, at least of the Phyllopharyngea, Colpodea, Nassophorea, and Oligohymenophorea.
Book
The third edition of The Ciliated Protozoa continues the innovative approach of the previous two editions, thoroughly documenting the progress in our understanding of the evolutionary diversification of these widely distributed eukaryotic microorganisms. The Glossary is considerably revised and expanded, serving as an illustrated 'subject index' of more than 700 terms. An introduction to the phylum is followed by chapters on the 11 classes. Each class chapter contains 7 sections: •taxonomic structure •life history and ecology •somatic structures •oral structures •division and morphogenesis •nuclei, sexuality, and life cycle •other features. The book includes new data on the ultrastructure of the somatic cortex of each class, molecular phylogenetics, ecology, and on other important aspects of ciliate biology. These new data are used, along with a novel conceptual approach, to rationalize a new system of classification for the phylum, presented in a major chapter on The Ciliate Taxa. The book includes an up-to-date bibliography of approximately 3,000 citations to both the 'classical' and recent literature, and both a Subject Index and a Systematic Index. This unique and timely book will serve as a comprehensive and authoritative reference work for students, teachers, and researchers who have an interest in the protozoa, and particularly the ciliates.
Article
RÉSUMÉ. RÉSUMÉ. Les relations de similarité ont été calculé es par analyse phé né tique entre 59 genres et espé ces, en considé rant 122 caractè res ultrastructuraux, morphologiques, stomatogé né tiques, nuclé aires ou de reproduction asexué e. L'é tude a d'abord porté sur 12 genres et espé ces de Colpodidé s car de nombreuses donné es ré centes sont maintenant disponibles sur ces Cilié s. Puis ľ'analyse a étéétendue, selon les mětrics normes, à 47 autres genres appartenant soit aux Kinetophragminophora, soit aux Oligohymenophora ou aux Poly-bymenophora. Sur la base des ré sultats obtenus, une nouvelle classification peut ětre avancé e. Trois sub-phylums sont discemables: Karyorelictophora, Kinetophragminophora, Hymenophora avec respectivement 1 classe (Karyorelictea), 4 classes (Colpodea; Hypo-stomea comprenant les Peniculida, Nassulida, Parapeniculida, Peritrichida; Spirotrichea avec les Hypotrichida, Clevelandellida, Het-erotrichida, Oligothchida; Hymenostomea avec Hymenostomatida et Apostomatida), 2 classes (Phyllopharyngea, Gymnostomea avec 2 sous-classes: Gymnostomia et Astomia).
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Stylonychia mytilus only differs from S. lemnae by its dorsal kineties 1–4, which are more bent apically and have a significantly greater number of cilia. These characters are difficult to recognize in vivo. Thus, we suggest that field biologists ought to employ the designation “member of the Stylonychia mytilus complex”. The cortical divisional morphogenesis is the same in the 4 clones investigated and described in detail for S. lemnae. The development of the dorsal ciliature and the division of the nuclear apparatus do not differ from those known of other Stylonychia species. The stomatogenesis begins with a proliferation of basal bodies close to the uppermost transverse cirrus. Three frontal-ventral-transverse (FVT) anlagen of the opisthe separate from the oral primordium and 3 from the right postoral ventral cirrus. In the proter anlage 1 originates from the parental undulating membranes, anläge 2 from the oral primordium of the opisthe, anlage 3 from the left posterior frontal cirrus, anlage 4 from the right posterior frontal cirrus, and anlagen 5 and 6 evolve from the right postoral ventral cirrus. The anlagen 1–6 generate 1-3-3-3-4-4 FVT-cirri.
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Concepts about specific relationships among various groups of protists are diverse and protist taxonomy is consequently unstable. In order to investigate the causes of this variety, data (mainly ultrastructural) relating to 198 characters of 25 species of heliozoa and other protozoa are analysed. Procedures are used which are compatible with numerical taxonomy (single linkage, complete linkage and group average cluster analyses), cladistic procedures (Camin--Sokal, Dollo and Wagner parsimony analyses) and evolutionary taxonomy (an intutive tree). The results are presented as branching diagrams. There is no complete congruence among any of the techniques, but all give similar results in some important aspects. The Wagner and Dollo parsimony analyses give those results which are most credible. The results corroborate the view that several major traditional taxa of protozoa (the heliozoa, flagellates, amoebae and filose amoebae) are polyphyletic and require revision. All of the analyses identify the following clusters: actinophryid heliozoa, centrohelid heliozoa, chrysophyte flagellates, actinomonad and pedinellid flagellates and nucleariid filose amoebae. As there is no disagreement, these are confirmed as monophyletic taxa. There is a strong suggestion for a close relationship between dimorphid flagellates and desmothoracid heliozoa. There is some support for the suggestion that the actinophryid heliozoa are more closely related to actinomonad helioflagellates than to other heliozoa. The results are summarized as an unrooted `true tree'. The lack of agreement among the analyses appears not to be due to a lack of rigour in analytical procedures, but to an inadequate supply of data. The paucity of data cannot be compensated for by the application of repeatable techniques. Most relationships among high level protist taxa are likely to be (currently) obscured by similar limitations. Ultrastructural data are well suited to mapping out the diversity of protozoa. Electron microscopy currently appears to be the most valuable technique for investigating problems of evolutionary relationships of protists. Various hurdles to the development of a natural (phylogenetic) classification of protists are discussed.
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The oral ciliature of Colpoda variabilis has been examined by serial thin sections. The left oral polykinetid consists of parallel rows of ciliated kinetosomes. The right oral polykinetid consists of a ventral part of ciliated kinetosomes in anarchic arrangement and a dorsal double row of ciliated kinetosomes. The existence of postciliary microtubules in association with each kinetosome makes it possible to determine the orientation of kinetosomes within the oral polykinetids. The orientation of kinetosomes in oral polykinetids and oral primordia is discussed and compared with the oral ciliature of Furgasonia, Paramecium and Tetrahymena. The left oral polykinetid is interpreted as consisting of adorai membranelies and the right oral polykinetid is interpreted as consisting of a stichodyad type of paroral membrane accompanied by a ciliary field in anarchic arrangement. A closer phylogenetic relationship between colpodid, nassulid and hymenostome ciliates is suggested.
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