Morphological and molecular characterization of a new ciliate Nyctotheroides grimi n. sp. (Armophorea, Clevelandellida) from Chinese frogs

Li, Ming; Hu, Guangran; Li, Can; Zhao, Weishan; Zou, Hong; Li, Wenxiang; Wu, Shangong; Wang, Guitang; Ponce-Gordo, Francisco

doi:10.1016/j.actatropica.2020.105531

Cited by 11 publications

(11 citation statements)

References 19 publications

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“…With regard to clevelandellids, the secondary structures of their nuclear rRNA molecules are well conserved and correspond to that of other eukaryotes (Lee & Gutell, 2012; Petrov et al, 2013, 2014). As expected, mutations are situated mainly in the hypervariable regions of the 18S rRNA molecule, especially in the V2, V4, and V7–V9 regions (Li et al, 2020; present study). Similarly to clevelandellids, the majority of mutations was detected within the hypervariable regions of the 18S rRNA molecule in the ciliate genera Haptophrya Stein, 1867, Plagiotoma Dujardin, 1841, and Trichodina Ehrenberg, 1830 (Obert et al, 2022; Rataj et al, 2022; Zhang et al, 2023).…”

Section: Discussionsupporting

confidence: 86%

“…A dominant number of mutations observed in the 5.8S rRNA molecule are situated in helix 9 (present study). Similarly, the majority of mutations was found in helix 9 in the clevelandellid genus Nyctotheroides Grassé, 1928 as well (Li et al, 2020). Higher variability of this helix was detected also in the genera Plagiotoma and Trichodina (Obert et al, 2022; Zhang et al, 2023).…”

Section: Discussionmentioning

confidence: 94%

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2D approach to reconstruct the evolutionary history of clevelandellids (Ciliophora, Armophorea) inhabiting the hindgut of the Panesthiinae cockroaches

Pecina

Vďačný

2023

Zoologica Scripta

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The ciliate order Clevelandellida unites endosymbionts of the digestive tract of a variety of invertebrates and vertebrates. In the present study, the primary and secondary structures of nuclear and hydrogenosomal rRNA molecules were employed to reconstruct the phylogenetic relationships and to estimate the divergence times of clevelandellids inhabiting the hindgut of the Panesthiinae cockroaches. The secondary structure information was incorporated in phylogenetic analyses using two different strategies, viz., indirectly through 2D‐guided alignments and directly through so‐called pseudo‐protein data. Nuclear and hydrogenosomal markers carried a consistent phylogenetic signal and robustly supported the monophyletic origin of the family Clevelandellidae as well as of its four genera. According to Bayesian relaxed molecular clock analyses, the last common ancestor (LCA) of the family Clevelandellidae very likely emerged during the Late Cretaceous in the Oriental region. Its descendants most likely expanded to Australia in concert with the Neogene colonization and radiation of their host Panesthiinae cockroaches. Taking into account the time‐calibrated phylogenies and the fact that early branching members of the order Clevelandellida inhabit the digestive tracts of amphibians, it is tempting to speculate that the LCA of the Clevelandellida evolved in ectothermic vertebrates. Amphibians could have brought clevelandellids to the land, where they may have been transmitted to the cockroach digestive tract upon feeding on amphibian faeces.

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Section: Discussionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 94%

2D approach to reconstruct the evolutionary history of clevelandellids (Ciliophora, Armophorea) inhabiting the hindgut of the Panesthiinae cockroaches

Pecina

Vďačný

2023

Zoologica Scripta

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“…Because of the enormous diversity of ciliates, only a few selected taxa from several groups were examined in terms of their ITS2 secondary structure. For instance, the heterotrichean genera Spirostomum Ehrenberg, 1833 (Shazib et al, 2016), and Condylostoma Bory de St. Vincent, 1824 (Chen et al, 2020); the pathogenic Balantidium coli Malmsten, 1857(Ponce-Gordo et al, 2011, as well as a number of free-living litostomateans (Rajter & Vďačný, 2017;Vďačný et al, 2012); the armophorean intestinal symbiont Nyctotheroides grimmi (Li et al, 2020) and variety of clevelandellids (Pecina & Vďačný, 2021); the oxytrichid Stylonychia lemnae Steinbruck & Schlegel, 1983(Coleman, 2005, the tinntinid Helicostomella subulata (Ehrenberg, 1833) Jörgensen, 1924 (Xu et al, 2012), various urostylid (Chen et al, 2021) and oligotrich (Li et al, 2013) spirotricheans; and oligohymenophoreans represented by 12 sessilids (Sun et al, 2010) and two mobilid (Rataj & Vďačný, 2021) genera, 16 astome species inhabiting the digestive tube of earthworms , a relatively diverse assemblage of scuticociliates (Gao et al, 2012(Gao et al, , 2013Miao et al, 2008) and, finally, two widely used model organisms, the peniculid Paramecium Müller, 1773, and the hymenostome Tetrahymena, with putative models proposed for P. tetraurelia (Ehrenberg, 1838) and T. tropicalis Nanney & McCoy, 1976(Coleman, 2005. The ITS2 secondary structures helped reliably distinguish most of the ciliate species studied but failed to discriminate distinct Spirostomum (Shazib et al, 2016(Shazib et al, , 2019, Trichodina (Rataj & Vďačný, 2021), and clevelandellid (Pecina & Vďačný, 2021) species.…”

Section: Introductionmentioning

confidence: 99%

Putative ITS2 secondary structure model and multi‐gene phylogenies of tetrahymenids (Ciliophora, Hymenostomatia) parasitizing planarians and crayfish worms

Rataj

Vďačný

2022

Zoologica Scripta

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Tetrahymena comprises over 80 free‐living as well as facultative or obligate histophagous species parasitizing especially invertebrates and fishes. Because of the comparatively high morphological conservativeness of tetrahymenids, their identification is primarily based on the gene coding for cytochrome c oxidase subunit I (COI). In addition to this mitochondrial barcoding marker, we tested here also the species discriminatory power of the highly variable nuclear ITS region, using the secondary structure of the ITS2 molecules and the compensatory base change (CBC) analysis. ITS2 secondary structures were proposed for 25 distinct ribotypes of 13 taxa, including three Tetrahymena species parasitizing planarians and crayfish worms, with the free‐energy minimization approach and the homology modelling. Although the majority of Tetrahymena species pairs can be reliably separated by one to six hemi‐CBCs localized especially in the third and fourth helix of the ITS2 molecules, some ITS region sequences might transcend species boundaries. In other words, intraspecies and interspecies p‐distances of ITS region sequences might overlap. This fact weakens the discriminatory power and the usage of the ITS region in the molecular taxonomy of Tetrahymena. On the other hand, there was always a distinct barcoding gap at about 4% sequence divergence in the case of the COI gene. Despite the slightly lower delimitation power of the ITS region, this molecular marker helped to recognize multiple previous misidentifications that were subsequently verified by comparing COI sequences.

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“…Studies on intestinal ciliates and opalinids of amphibians are limited to few geographical areas and host species. Nevertheless, identification to genus level was possible [32][33][34]. Vouchers specimens of each taxon were deposited at the Zoologisches Museum Hamburg, LIB-Leibniz Institut für die Analyse des Biodiversitätswandels, Germany.…”

Section: Morphological Identification Of Parasites and Endocommensalsmentioning

confidence: 99%

Component Endoparasite Communities Mirror Life-History Specialization in Syntopic Reed Frogs (Hyperolius spp.)

et al. 2021

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Most of our knowledge on the processes structuring parasite communities in amphibians originate from temperate-zone taxa, whereas Afrotropical communities have been neglected so far. We found evidence that ecological fitting of the hosts and, probably, differential immune response may influence the variation in parasite species richness, prevalence, and infestation intensity of East African frogs Hyperolius kivuensis and H. viridiflavus. The most closely related host species share the same macrohabitat (that implies the same pool of potential parasites), but differ in microhabitat preference, so that a comparative analyses of syntopic and allopatric populations is expedient to reveal ecological fitting. We detected 11 parasite species (one annelid, four nematodes, five trematodes, one cestode) and two endocommensal species (protozoans). The component parasite communities included 4–5 helminth species in H. kivuensis and 6–8 in the more aquatic H. viridiflavus, supporting the hypothesis that trematode diversity increases with the amount of time spent in water. Five parasite species (Orneoascaris chrysanthemoides, Clinostomum chabaudi, an undetermined echinostomatid) and two protozoans (Nyctotheroides sp., and Protoopalina sp.) are shared among the syntopic amphibian populations. This finding indicates a similar susceptibility of these amphibians to infestation from the local parasite pool. Yet, the low prevalence of single- and multi-species infestations in H. kivuensis indicates that parasite clearing by its immune response is probably more effective and prominent than in H. viridiflavus. Therefore, H. viridiflavus suffered from significantly reduced short-term survival due to the infection. Thus, we conclude that the processes structuring component parasite communities in amphibians do not differ generally between temperate-zone and Afrotropical host species, but they do in the magnitude of ecological fitting.

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Morphological and molecular characterization of a new ciliate Nyctotheroides grimi n. sp. (Armophorea, Clevelandellida) from Chinese frogs

Cited by 11 publications

References 19 publications

2D approach to reconstruct the evolutionary history of clevelandellids (Ciliophora, Armophorea) inhabiting the hindgut of the Panesthiinae cockroaches

2D approach to reconstruct the evolutionary history of clevelandellids (Ciliophora, Armophorea) inhabiting the hindgut of the Panesthiinae cockroaches

Putative ITS2 secondary structure model and multi‐gene phylogenies of tetrahymenids (Ciliophora, Hymenostomatia) parasitizing planarians and crayfish worms

Component Endoparasite Communities Mirror Life-History Specialization in Syntopic Reed Frogs (Hyperolius spp.)

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