On four epibiotic peritrichous ciliates (Protozoa, Ciliophora) found in Lake Weishan Wetland: morphological and molecular data support the establishment of a new genus, Parapiosoma gen. nov., and two new species

Tong Wu1,2, Ting Cheng2, Xiao Cao3, Yaohan Jiang2, Khaled A. S. Al-Rasheid4, Alan Warren5, Zhe Wang1, Borong Lu2
1Marine College, Shandong University, Weihai, China
2Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China
3Weishan Fishery Development Service Center, Jining, China
4Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia
5Department of Life Sciences, Natural History Museum, London, UK

Tóm tắt

During a study on the diversity of ciliated protists in Lake Weishan Wetland, the largest wetland in northern China, four epibiotic sessilid peritrichs were isolated from aquatic host animals. Two of them, i.e., Epistylis cambari Kellicott, 1885 and Epistylis lwoffi Fauré-Fremiet, 1943, were known species whereas the other two, i.e., Parapiosoma typicum gen. nov., sp. nov. and Orborhabdostyla gracilis sp. nov., are new to science. The new genus Parapiosoma gen. nov. is characterized by its branched non-contractile stalk, everted peristomial lip, obconical macronucleus and transverse silverlines. Two species are assigned to the new genus, namely Parapiosoma typicum sp. nov. and Parapiosoma gasterostei (Fauré-Fremiet, 1905) comb. nov. Morphologically, P. typicum sp. nov. is recognized by its goblet-shaped zooids, single-layered peristomial lip, dichotomously branched stalk, and infundibular polykinety 3 (P3) containing three equal-length rows. Orborhabdostyla gracilis sp. nov. is characterized by its slender zooid, curved macronucleus, and three equal-length rows in infundibular P3. Improved diagnoses and redescriptions of E. cambari and E. lwoffi are provided including, for the first time, data on the ciliature of E. cambari. Phylogenetic analyses based on SSU rDNA, ITS1-5.8S rDNA -ITS2, and LSU rDNA sequence data strongly support the assertion that the family Epistylididae comprises morphospecies with different evolutionary lineages and indicate that Parapiosoma gen. nov. may represent a new taxon at family level.

Từ khóa


Tài liệu tham khảo

Banina NN (1968) Apiosoma from freshwater fishes in the European part of the Soviet Union (systematic review). Acta Protozool 6:245–262

Biegel M (1954) Beitrag zur Peritrichenfauna der umgebung von Erlangen. Fischer

Blanchard R (1885) Sur un infusoire peritriche ectoparasite. Bull Soc Zool Fr 10:277–280

Blažeković-Dimovska D, Stojanovski S (2020) First record of Apiosoma piscicola (Blanchard, 1885) (Ciliophora: Epistylididae) in common carp (Cyprinus carpio Linnaeus, 1758) (Pisces: Cyprinidae) from aquaculture facilities in North Macedonia. Ann Parasitol 66:227–230

Campello-Nunes PH, Woelfl S, da Silva-Neto ID, Paiva TDS, Fernández LD (2022) Checklist, diversity and biogeography of ciliates (Ciliophora) from Chile. Eur J Protistol 84:125892

Canals O, Salvadó i Cabré HH (2016) Description of Epistylis camprubii n. sp., a species highly tolerant to ammonium and nitrite. Acta Protozool 55:7–18

Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

Chen LL, Ren YJ, Han K, Stoeck T, Jiang JM, Pan HP (2022) Re-description and molecular phylogeny of the free-swimming peritrichs Hastatella radians Erlanger, 1890 and H. aesculacantha Jarocki & Jakubowska, 1927 (Ciliophora, Peritrichia) from China. Eur J Protistol 84:125891

Chi Y, Chen XR, Li YQ, Wang CD, Zhang TT, Ayoub A, Warren A, Song WB, Wang YY (2021) New contributions to the phylogeny of the ciliate class Heterotrichea (Protista, Ciliophora): analyses at family-genus level and new evolutionary hypotheses. Sci China Life Sci 64:606–620

Chi Y, Wang Z, Ye TT, Wang Y, Zhao JL, Song WB, Bourland WA, Chen XR (2022) A new contribution to the taxonomy and phylogeny of the ciliate genus Spirostomum (Alveolata, Ciliophora, Heterotrichea), with comprehensive descriptions of two species from wetlands in China. Water Biol Sec 1:100031

Clamp JC, Williams D (2006) A molecular phylogenetic investigation of Zoothamnium (Ciliophora, Peritrichia, Sessilida). J Eukaryot Microbiol 53:494–498

Claparède É, Lachmann J (1858) Études sur les infusoires et les rhizopodes, vol I. Kessmann

Corliss JO (1979) The ciliated protozoa: characterization, classification and guide to the literature, 2nd edn. Pergamon Press, Oxford, UK

Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772

Fauré-Fremiet E (1905) La structure de l’appariel fixateur chez les vorticellidae. Arch Protistenk 6:207–226

Fauré-Fremiet E (1943) Commensalisme et adaptation chez une vorticellide Epistylis lowffi n. sp. Bull Soc Zool Fr 68:154–158

Foissner W (1983) Morphologie und Infraciliatur zweier ectocommensaler Ciliaten (Protozoa: Ciliophora) von Cyprinus carpio L. (Pisces; Cypriniformes): Heteropolaria lwoffi (Fauré-Fremiet, 1943) (Peritrichida: Epistylididae) und ihr Predator Pseudoamphileptus macrostoma (Chen, 1955) nov. gen. (Pleurostomatida: Amphileptidae). Zool Jahrb Abt Syst 110:399–418

Foissner W (2014) An update of ‘basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa’. Int J Syst Evol Microbiol 64:271–292

Foissner W, Schubert G (1977) Morphologe der Zooide und Schwarmer von Heteropolaria colisarum gen. nov., spec. nov. (Ciliata, Peritrichide), einer symphorioten Epistylidae von Calisa fasciata (Anabantoidei, Belontiidae). Acta Protozool 16:231–247

Foissner W, Hoffman GL, Mitchell AJ (1985) Heteropolaria colisarum Foissner & Schubert, 1977 (Protozoa: Epistylididae) of North American freshwater fishes. J Fish Dis 8:145–160

Foissner W, Berger H, Kohmann F (1992) Taxonomische und okologische revision der ciliaten des saprobiensystems. Band II: peritrichia, heterotrichida, odontostomatida. Informationsberichte des Bayer. Landesamtes für Wasserwirtschaft, pp 1–502

Foissner W, Berger H, Schaumburg J (1999) Identification and ecology of limnetic plankton ciliates. Informationsberichte des Bayer. Landesamtes für Wasserwirtschaft, pp 1–793

Foissner W, Blake N, Wolf K, Breiner H, Stoeck T (2010) Morphological and molecular characterization of some peritrichs (Ciliophora: Peritrichida) from tank bromeliads, including two new genera: Orborhabdostyla and Vorticellides. Acta Protozool 22:291–319

Gao F, Warren A, Zhang QQ, Gong J, Miao M, Sun P, Xu DP, Huang J, Yi ZZ, Song WB (2016) The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (Eukaryota, Alveolata). Sci Rep 6:24874

Gentekaki E, Kolisko M, Gong YC, Lynn D (2017) Phylogenomics solves a long-standing evolutionary puzzle in the ciliate world: the subclass Peritrichia is monophyletic. Mol Phylogenet Evol 106:1–5

Gómez F, Wang L, Lin S (2018) Morphology and molecular phylogeny of peritrich ciliate epibionts on pelagic diatoms: Vorticella oceanica and Pseudovorticella coscinodisci sp. nov. (Ciliophora, Peritrichia). Protist 169:268–279

Gong J, Kim SJ, Kim SY, Min GS, Roberts DM, Warren A, Choi JK (2007) Taxonomic redescriptions of two ciliates, Protogastrostyla pulchra n. g., n. comb. and Hemigastrostyla enigmatica (Ciliophora: Spirotrichea, Stichotrichia), with phylogenetic analyses based on 18S and 28S rRNA gene sequences. J Eukaryot Microbiol 54:468–478

Greenwood SJ, Sogin ML, Lynn DH (1991) Phylogenetic relationships within the class Oligohymenophorea, phylum Ciliophora, inferred from the complete small subunit rRNA gene sequences of Colpidium campylum, Glaucoma chattoni, and Opisthonecta henneguyi. J Mol Evol 33:163–174

Hu XZ, Lin XF, Song WB (2019) Ciliate atlas: species found in the South China Sea. Science Press, Beijing, China

Huang JB, Zhang TT, Zhang QQ, Li Y, Warren A, Pan HB, Yan Y (2018) Further insights into the highly derived haptorids (Ciliophora, Litostomatea): phylogeny based on multigene data. Zool Scr 47:231–242

Irwin NA, Lynn DH (2015) Molecular phylogeny of mobilid and sessilid ciliates symbiotic in Eastern Pacific limpets (Mollusca: Patellogastropoda). J Eukaryot Microbiol 62:543–552

Jerome CA, Lynn DH, Simon EM (1996) Description of Tetrahymena empidokyrea n. sp., a new species in the Tetrahymena pyriformis sibling species complex (Ciliophora, Oligohymenophorea), and an assessment of its phylogenetic position using small-subunit rRNA sequences. Can J Zool 74:1898–1906

Ji DD, Kim JH, Shazib SUA, Sun P, Li LQ, Shin MK (2015) Two new species of Zoothamnium (Ciliophora, Peritrichia) from Korea, with new observations of Z. parahentscheli Sun et al., 2009. J Eukaryot Microbiol 62:505–518

Jiang CQ, Shi XL, Liu GJ, Jiang Y, Warren A (2016) Morphology and molecular phylogeny of two freshwater peritrich ciliates, Epistylis chlorelligerum Shen, 1980 and Epistylis chrysemydis Bishop & Jahn, 1941 (Ciliophora, Peritrichia). J Eukaryot Microbiol 63:16–26

Jiang CQ, Wang GY, Xiong J, Yang WT, Sun ZY, Feng JM, Warren A, Miao W (2019) Insights into the origin and evolution of Peritrichia (Oligohymenophorea, Ciliophora) based on analyses of morphology and phylogenomics. Mol Phylogenet Evol 132:25–35

Kahl A (1935) Urtiere oder Protozoa. I. Wimpertiere oder Ciliata (Infusoria) 4. Peritricha und Chonotricha. Tierwelt Dtl 30:651–886

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

Kellicott DS (1885) Observations on some fresh-water infusoria: with descriptions of a few species regarded as new. Proc Am Soc Microsc 7:38–47

Kühner S, Simão TL, Safi LSL, Gazulha FB, Eizirik E, Utz LRP (2016) Epistylis portoalegrensis n. sp. (Ciliophora, Peritrichia): a new freshwater ciliate species from southern Brazil. J Eukaryot Microbiol 63:93–99

Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

Li LF, Song WB, Warren A, Shin MK, Chen ZG, Ji DD, Sun P (2008a) Reconsideration of the phylogenetic positions of five peritrich genera, Vorticella, Pseudovorticella, Zoothamnopsis, Zoothamnium, and Epicarchesium (Ciliophora, Peritrichia, Sessilida), based on small subunit rRNA gene sequences. J Eukaryot Microbiol 55:448–456

Li M, Wang JG, Zhu DL, Gu ZM, Zhang JY, Gong XN (2008b) Study of Apiosoma piscicola (Blanchard 1885) occurring on fry of freshwater fishes in Hongze, China with consideration of the genus Apiosoma. Parasitol Res 102:931–937

Li M, Sun ZY, Wang C, Zhang L (2016) Ultrastructural study of Apiosoma piscicola Blanchard, 1885 (Subclass: Peritrichia) on Tachysurus fulvidraco from China. J Parasitic Dis 40:1429–1434

Liao WY, Campello-Nunes PH, Gammuto L, Viana TA, de Oliveira MR, da Silva PT, da Silva-Neto ID, Modeo L, Petroni G (2021) Incorporating mitogenome sequencing into integrative taxonomy: the multidisciplinary redescription of the ciliate Thuricola similis (Peritrichia, Vaginicolidae) provides new insights into the evolutionary relationships among Oligohymenophorea subclasses. Mol Phylogenet Evol 158:107089

Lom J (1964) The morphology and morphogenesis of the buccal ciliary organelles in some peritrichous ciliates. Arch Protistenk 107:131–162

Lom J (1966) Sessiline peritrichs from the surface of some freshwater fishes. Folia Parasitol 13:36–56

Lom J, de Puytorac P (1994) Sous-classe des Peritrichia Stein, 1859. Traité Zool 2:681–737

Lom J, Vávra J (1961) Epistylis lwoffi (?) from the skin of perches. Acta Soc Zool Bohemoslov 4:273–276

Lu BR, Shen Z, Zhang QQ, Hu XZ, Warren A, Song WB (2020) Morphology and molecular analyses of four epibiotic peritrichs on crustacean and polychaete hosts, including descriptions of two new species (Ciliophora, Peritrichia). Eur J Protistol 73:125670

Lu BR, Hu XZ, Warren A, Song WB, Yan Y (2023) From oral structure to molecular evidence: new insights into the evolutionary phylogeny of the ciliate order Sessilida (Protista, Ciliophora), with the establishment of two new families and new contributions to the poorly studied family Vaginicolidae. Sci China Life Sci. https://doi.org/10.1007/s11427-022-2268-2

Lynn DH (2008) The ciliated protozoa characterization, classification, and guide to the literature, 3rd edn. Springer, Dordrecht, Netherlands, pp 1–27

Ma MZ, Xu Y, Yan Y, Li YQ, Warren A, Song WB (2021) Taxonomy and molecular phylogeny of four karyorelictid species belonging to the genera Apotrachelocerca and Tracheloraphis (Protozoa: Ciliophora), with descriptions of two new species. Zool J Linn Soc 192:690–709

Ma MZ, Li Y, Maurer-Alcalá XX, Wang YY, Yan Y (2022a) Deciphering phylogenetic relationships in class Karyorelictea (Protista, Ciliophora) based on updated multi-gene information with establishment of a new order Wilbertomorphida n. ord. Mol Phylogenet Evol 169:107406

Ma MZ, Liu YJ, Xu Y, Lu BR, Li YQ, Al-Farraj SA, Petroni G, Song WB, Yan Y (2022b) Molecular phylogeny and taxonomy of four Remanella species (Protozoa, Ciliophora): a flagship genus of karyorelictean ciliates, with descriptions of two new species. Zool Res 43:827–842

Matthes D, Guhl W (1973) Sessile ciliaten der flusskrebse. Protistologica 9:459–470

Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499

Méndez-Sánchez D, Pomahač O, Rotterová J, Bourland W, Čepička I (2022) Diversity and phylogenetic position of Bothrostoma Stokes, 1887 (Ciliophora: Metopida), with description of four new species. Protist 173:125887

Miao W, Yu YH, Shen YF (2001) Phylogenetic relationships of the subclass Peritrichia (Oligohymenophorea, Ciliophora) with emphasis on the genus Epistylis, inferred from small subunit rRNA gene sequences. J Eukaryot Microbiol 48:583–587

Miao W, Fen WS, Yu YH, Zhang XY, Shen YF (2004) Phylogenetic relationships of the subclass Peritrichia (Oligohymenophorea, Ciliophora) inferred from small subunit rRNA gene sequences. J Eukaryot Microbiol 51:180–186

Nenninger U (1948) Die peritrichen der umgebung von Erlangen mit besonderer berücksichtigung ihrer wirtsspezifittät. Zool Jahrb 77:169–266

Omar A, Yeo JH, Jung JH (2022) A new “flagship” ciliate, Pseudostylonychia obliquocaudata n. gen., n. sp. (Ciliophora, Hypotricha), from South Korea. Eur J Protistol 84:125893

Penard E (1922) Études sur les infusoires d’eau douce. Georg & Cie, Genève

Precht H (1935) Epizoen der Kieler Bucht. Nova Acta Leopold 3:405–474

Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larger B, Liu L, Suchard MA, Hurlsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

Safi LSL, Tang KW, Carnegie RB (2022) Investigating the epibiotic peritrich Zoothamnium intermedium Precht, 1935: seasonality and distribution of its relationships with copepods in Chesapeake Bay (USA). Eur J Protistol 84:125880

Scheubel J (1973) Die sessilen ciliaten unserer süsswasserfische unter besonderer berücksichtigung der gattung Apiosoma Blanchard. Zool Jahrb Abt Syst Geogr Biol Tiere 100:1–63

Schödel H (1987) Seßhafte Wimpertierchen (Peritricha, Chonotricha, Suctoria) auf Asellus aquaticus und Gammariden (Doctoral dissertation).

Schödel H (2018) Kompendium der auf Wirbellosen epizoisch lebenden limnischen sessilen Peritrichia (Ciliophora) West-, Mittel- und Osteuropas. Denisia 41:47–294

Shen YF, Gu MR (2016) Fauna sinica. Invertebrata: Ciliophora: Oligohymenophorea: Peritrichida, vol 45. Science Press, Beijing

Sommer G (1951) Die peritrichen ciliaten des Großen Plöner Sees. Arch Hydrobiol 44:349–440

Song WB, Zhao YJ, Xu KD, Hu XZ, Gong J (2003) Pathogenic protozoa in mariculture. Science Press, Beijing, China

Song WB, Warren A, Hu XZ (2009) Free–living ciliates in the Bohai and Yellow Seas. Science Press, Beijing, China

Song WY, Luo X, Chi Y, Al-Farraj SA, Shao C (2022) Ontogenesis and systematic position of a new hypotrichous ciliate, Chaetospira sinica sp. nov., with an improved diagnosis of the poorly defined family Chaetospiridae Jankowski, 1985 (Protozoa, Ciliophora, Hypotrichia). Mar Life Sci Technol 4:513–526

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post–analysis of large phylogenies. Bioinformatics 30:1312–1313

Stein F (1854) Die Infusionsthiere auf ihre Entwickelungsgeschichte. Engelmann, Leipzig

Stiller J (1963) Zur limnologie der natrongewässer ungarns I. Der natronsee nagyszek und seine peritrichenfauna. Int Rev Gesamten Hydrobiol Hydrogr 48:603–612

Stiller J (1971) Szájkoszorús csillósok–Peritricha. Fauna Hung 105:1–245

Sun P, Clamp J, Xu DP, Huang B, Shin MK (2016) An integrative approach to phylogeny reveals patterns of environmental distribution and novel evolutionary relationships in a major group of ciliates. Sci Rep 6:1–12

Sun P, Al-Farraj SA, Warren A, Ma HG (2017) Morphology of four new solitary sessile peritrich ciliates from the Yellow Sea, China, with description of an unidentified species of Paravorticella (Ciliophora, Peritrichia). Eur J Protistol 57:73–84

Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

Utz LRP, Farias AC, Freitas EC, Araujo GO (2014) Description of Epistylis riograndensis n. sp. (Ciliophora: Peritrichia) found in an artificial lake in southern Brazil. Zootaxa 3869:557–564

Viljoen S, Van As JG (1985) Sessile peritrichs (Ciliophora: Peritricha) from freshwater fish in the Transvaal, South Africa. Afr Zool 20:79–96

Wang XY, Ji DD (2019) Morphological and molecular identification of a new ciliate, Zoothamnium palmphlatum nov. spec. (Ciliophora, Peritrichia) from north China. J Eukaryot Microbiol 66:670–679

Wang Z, Zhou T, Guo QX, Gu ZM (2017) Description of a new freshwater ciliate Epistylis wuhanensis n. sp. (Ciliophora, Peritrichia) from China, with a focus on phylogenetic relationships within family Epistylididae. J Eukaryot Microbiol 64:394–406

Wang Z, Wu T, Lu BR, Chi Y, Zhang X, Al-Farraj SA, Song WB, Warren A, Li LF, Wang CD (2021) Integrative studies on a new ciliate Campanella sinica n. sp. (Protista, Ciliophora, Peritrichia) based on the morphological and molecular data, with notes on the phylogeny and systematics of the family Epistylididae. Front Microbiol 12:718757

Wang XY, Jiang CQ, Gu SY, Liu ZC, Xiong J, Warren A, Miao W (2022a) Large-scale phylogenetic analysis provides insights into the diversification and evolution of sessilid peritrich ciliates (Protista: Ciliophora). J Eukaryot Microbiol 69:e12950

Wang Z, Chi Y, Li T, Song WY, Wang YF, Wu T, Zhang GAT, Liu YJ, Ma HG, Song WB, Al-Rasheid KAS, Warren A, Lu BR (2022b) Biodiversity of freshwater ciliates (Protista, Ciliophora) in the Lake Weishan Wetland, China: the state of the art. Mar Life Sci Technol 4:429–451

Wang Z, Feng XT, Li LF, Al-Rasheid KA, Warren A, Wang CD, Gu ZM (2022c) New considerations on the phylogeny of Sessilida (Protista: Ciliophora: Peritrichia) based on multiple-gene information, with emphasis on colonial taxa. Mar Life Sci Technol 4:569–583

Wang Z, Wu T, Mu CJ, Wang Y, Lu BR, Warren A, Wang CD (2022d) The taxonomy and molecular phylogeny of two epibiotic colonial peritrich ciliates (Ciliophora, Peritrichia). Eur J Protistol 86:125921

Warren A (1986) A revision of the genus Vorticella (Ciliophora: Peritrichida). Bull Br Mus Nat Hist (zool) 50:1–57

Wilbert N (1975) Eine verbesserte Technik der Protargol Impräg-nation für Ciliaten. Mikrokosmos 64:171–179

Williams D, Clamp JC (2007) A molecular phylogenetic investigation of Opisthonecta and related genera (Ciliophora, Peritrichia, Sessilida). J Eukaryot Microbiol 54:317–323

Wu T, Li YQ, Lu BR, Shen Z, Song WB, Warren A (2020) Morphology, taxonomy and molecular phylogeny of three marine peritrich ciliates, including two new species: Zoothamnium apoarbuscula n. sp. and Z. apohentscheli n. sp. (Protozoa, Ciliophora, Peritrichia). Mar Life Sci Technol 2:31–40

Wu T, Li YQ, Zhang TT, Hou J, Mu CJ, Warren A, Lu BR (2021a) Morphology and molecular phylogeny of three Epistylis species found in freshwater habitats in China, including the description of E. foissneri n. sp. (Ciliophora, Peritrichia). Eur J Protistol 78:125767

Wu T, Wang Z, Duan LL, El-Serehy H, Al-Farraj SA, Warren A, Liu YJ, Wang CD, Lu BR (2021b) The morphology, taxonomy, and phylogenetic analyses of five freshwater colonial peritrich ciliates (Alveolata, Ciliophora), including the descriptions of two new species. Front Microbiol 12:718821

Wu T, Liu YJ, Liu Y, Lu BR, Cao X, Hao S, Al-Farraj SA, Warren A, Zhang TT, Wang Z (2022a) Integrative studies on three epibiotic Epistylis species (Protozoa, Ciliophora, Peritrichia) in Lake Weishan Wetland, northern China, including the establishment of a new species. Protist 173:125909

Wu T, Wang Z, Lu BR, Lei JT, Al-Rasheid KAS, Sheng YL (2022b) New contribution to the peritrichous genus Ophrydium (Protista, Ciliophora) with notes on the morphology, taxonomy, and phylogeny of a well-known species Ophrydium crassicaule Penard, 1922. J Eukaryot Microbiol 69:e12900

Ye TT, Jiang YH, Chen SC, Xu YX, Li LF, Shin MK, Chen XR (2022) The widely reported but poorly studied ciliate family Folliculinidae (Protozoa, Ciliophora, Heterotrichea): a revision with notes on its taxonomy, morphology and phylogenetic relationships. Mar Life Sci Technol 4:471–492

Zhang GAT, Zhao Y, Chi Y, Warren A, Pan HB, Song WB (2022a) Updating the phylogeny and taxonomy of pleurostomatid ciliates (Protista: Ciliophora) with establishment of a new family, a new genus and two new species. Zool J Linn Soc 196:105–123

Zhang X, Lu XT, Chi Y, Jiang YH, Wang CD, Al-Farraj SA, Vallesi A, Gao F (2022b) Timing and characteristics of nuclear events during conjugation and genomic exclusion in Paramecium multimicronucleatum. Mar Life Sci Technol 4:317–328

Zhou T, Wang Z, Yang H, Gu ZM (2019a) Two new colonial peritrich ciliates (Ciliophora, Peritrichia, Sessilida) from China: with a note on taxonomic distinction between Epistylididae and Operculariidae. Eur J Protistol 70:17–31

Zhou T, Wang Z, Yang H, Gu ZM (2019b) Morphological and molecular identification of epibiontic sessilid Epistylis semiciculus n. sp. (Ciliophora, Peritrichia) from Procambarus clarkia (Crustacea, Decapoda) in China. Int J Parasitol: Parasit Wildl 10:289–298

Zhuang Y, Clamp JC, Yi ZZ, Ji DD (2018) Phylogeny of the families Zoothamniidae and Epistylididae (Protozoa: Ciliophora: Peritrichia) based on analyses of three rRNA–coding regions. Mol Phylogenet Evol 118:99–107