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Ultrastructure of Diophrys appendiculata and new systematic consideration of the euplotid family Uronychiidae (Protista, Ciliophora)

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Abstract

The ultrastructure of ciliates carries important cytological, taxonomical, and evolutionary signals for these single-celled eukaryotic organisms. However, little ultrastructural data have been accumulated for most ciliate groups with systematic problems. In the present work, a well-known marine uronychiid, Diophrys appendiculata, was investigated using electron microscopy and a comparison with, and a discussion considering, phylogenetic analyses were made. The new findings primarily show that: (i) this species lacks the typical alveolar plate, bears cortical ampule-like extrusomes, and has microtubular triads in the dorsal pellicle, and thus exhibits some ultrastructural features in common with most of its previously studied congeners; (ii) each adoral membranelle before the level of frontal cirrus II/2 contains three rows of kinetosomes and each membranelle after the level of frontal cirrus II/2 contains four rows, which might be related with morphogenesis and could be considered as a distinctive character of Diophrys; (iii) some structural details of the buccal field, such as the extra-pellicular fibrils, pellicle, pharyngeal disks and microtubular sheet, were documented. In addition, based on the ultrastructural comparison of representatives, we discuss the differentiation between the subfamilies Diophryinae and Uronychiinae. A hypothetical systematic relationship of members in the order Euplotida based on a wide range of data is also provided.

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Data availability

A voucher slide (registration number: DJY2018030701) with protargol-stained specimens of the Qingdao population of Diophrys appendiculata has been deposited into the collection of the Laboratory of Protozoology (OUC), Qingdao, China. The SSU rDNA sequence of Diophrys appendiculata Qingdao population has been deposited in the GenBank database with accession number OK039190.

References

  • Adl SM, Simpson AG, Lane CE, Lukes J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, Le Gall L, Lynn DH, McManus H, Mitchell EA, Mozley-Stanridge SE, Parfrey LW, Pawlowski J et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–493

    Article  PubMed  PubMed Central  Google Scholar 

  • Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66:4–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Asghar U, Chi Y, Gao Y, Lu B, Jiang Y, Gong R, Ma H, Al-Rasheid KA, Gao F (2021) Morphogenesis of the ciliature during sexual process of conjugation in the ciliated protist Euplotes raikovi. Front Mar Sci 7:1165

    Article  Google Scholar 

  • Bai Y, Wang R, Song W, Suzuki T, Hu X (2020) Redescription of five tintinnine ciliates (Alveolata: Ciliophora: Oligotrichea) from coastal waters of Qingdao, China. Mar Life Sci Technol 2:209–221

    Article  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardele CF, Huttenlauch I, Schoppmann H (1986) The ciliate cortex studied by TEM and SEM cryofracture techniques. Symp Biol Hung 33:115–124

    Google Scholar 

  • Borror AC (1972) Revision of the order Hypotrichida (Ciliophora, Protozoa). J Protozool 19:1–23

    Article  CAS  PubMed  Google Scholar 

  • Borror AC, Hill BF (1995) The order Euplotida (Ciliophora): taxonomy, with division of Euplotes into several genera. J Eukaryot Microbiol 42:457–466

    Article  Google Scholar 

  • Chen Z, Song W (2002) Characterization and identification of the Diophrys species (Protozoa, Ciliophora, Hypotrichida) based on RAPD fingerprinting and ARDRA riboprinting. Eur J Protistol 38:383–391

    Article  Google Scholar 

  • Chen X, Ma H, Al-Rasheid KAS (2014) Taxonomic description of a new marine ciliate, Euplotes qingdaoensis n. sp. (Ciliophora: Euplotida). Chin J Oceanol Limnol 32:426–432

    Article  CAS  Google Scholar 

  • Chen X, Jiang Y, Gao F, Zheng W, Krock TJ, Stover NA, Lu C, Katz LA, Song W (2019) Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors. Mol Ecol Resour 19:1292–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corliss JO (1979) The ciliated protozoa: characterization, classification, and guide to the literature, vol 455. Pergamon Press, Oxford

    Google Scholar 

  • Curds CR (1975) A guide to the species of the genus Euplotes (Hypotrichida, Ciliatea). Bull Br Mus Nat Hist (Zool) 28:1–61

    Google Scholar 

  • Curds CR, Wu ICH (1983) A review of the Euplotidae (Hypotrichida, Ciliophora). Bull Br Mus Nat Hist (Zool) 44:191–247

    Google Scholar 

  • Dallai R, Luporini P (1981) Membrane specializations in the ciliate Euplotes crassus at the site of interaction of the ampules with the plasma membrane. Eur J Cell Biol 23:280–285

    CAS  PubMed  Google Scholar 

  • de Puytorac P, Grain J, de Santa R, Rosa M (1976) A propos de l’ultrastructure corticale du cilié hypotriche Stylonychia mytilus Ehrbg., 1838: les caracteristiques du cortex buccal adoral et paroral des Polyhymenophora Jankowski, 1967. Trans Am Microsc Soc 95:327–345

    Article  Google Scholar 

  • Di Giuseppe G, Erra F, Paolo Frontini F, Dini F, Vallesi A, Luporini P (2014) Improved description of the bipolar ciliate, Euplotes petzi, and definition of its basal position in the Euplotes phylogenetic tree. Eur J Protistol 50:402–411

    Article  PubMed  Google Scholar 

  • Dong J, Li L, Fan X, Ma H, Warren A (2019) Two Urosoma species (Ciliophora, Hypotrichia): a multidisciplinary approach provides new insights into their ultrastructure and taxonomy. Eur J Protistol 72:125661

    Article  PubMed  Google Scholar 

  • Dong J, Chen X, Liu Y, Ni B, Fan X, Li L, Warren A (2020a) An integrative investigation of Parabistichella variabilis (Protista, Ciliophora, Hypotrichia) including its general morphology, ultrastructure, ontogenesis, and molecular phylogeny. J Eukaryot Microbiol 67:566–582

    Article  CAS  PubMed  Google Scholar 

  • Dong J, Fan X, Zhang T, Al-Farraj SA, Stoeck T, Ma H, Li L (2020b) Ultrastructural features of an abundant and ubiquitous marine ciliate, Uronychia binucleata (Protista, Ciliophora, Euplotida). Front Mar Sci 7:604487

    Article  Google Scholar 

  • Fan Y, Warren A, Al-Farraj SA, Chen X, Shao C (2013) Morphology and SSU rRNA gene-based phylogeny of two Diophrys-like ciliates from northern China, with notes on morphogenesis of Pseudodiophrys nigricans (Protozoa, Ciliophora). J Morphol 274:395–403

    Article  CAS  PubMed  Google Scholar 

  • Fauré-Fremiet E, André J (1968) Fine structure of Euplotes eurystomus (Wrz). Arch Anat Microsc Morphol Exp 57:53–78

    PubMed  Google Scholar 

  • Fischer-Defoy D, Hausmann K (1981) Microtubules, microfilaments, and membranes in phagocytosis: structure and function of the oral apparatus of the ciliate Climacostomum virens. Differentiation 20:141–151

    Article  Google Scholar 

  • Foissner W (1978) Euplotes moebiusi f. quadricirratus (Ciliophora, Hypotrichida) I. Die feinstruktur des cortex und der argyrophilen strukturen. Arch Protistenk 120:86–117

    Article  Google Scholar 

  • Fotedar R, Stoeck T, Filker S, Fell JW, Agatha S, Al Marri M, Jiang J (2016) Description of the halophile Euplotes qatarensis nov. spec. (Ciliophora, Spirotrichea, Euplotida) isolated from the Hypersaline Khor Al-Adaid Lagoon in Qatar. J Eukaryot Microbiol 63:578–590

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao Y, Gong R, Jiang Y, Pan B, Li Y, Warren A, Jiang J, Gao F (2020) Morphogenetic characters of the model ciliate Euplotes vannus (Ciliophora, Spirotrichea): notes on cortical pattern formation during conjugational and postconjugational reorganization. Eur J Protistol 73:125675

    Article  PubMed  Google Scholar 

  • Gliddon R (1966) Ciliary organelles and associated fibre systems in Euplotes eurystomus (Ciliata, Hypotrichida): I. Fine Struct J Cell Sci 1:439–448

    Article  CAS  Google Scholar 

  • Gong ZW, Fan XP, Ma R, Ni B (2018) Ultrastructure of vegetative cells and resting cysts, and live observations of the encystation and excystation processes in Diophrys oligothrix Borror, 1965 (Protista, Ciliophora). J Morphol 279:1397–1407

    Article  CAS  PubMed  Google Scholar 

  • Gong R, Jiang Y, Vallesi A, Gao Y, Gao F (2020) Conjugation in Euplotes raikovi (Protista, Ciliophora): new insights into nuclear events and macronuclear evelopment from micronucleate and amicronucleate cells. Microorganisms 8:162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong R, Chi Y, Shao C, Yuan Q, Li Y, Warren A, Wang Y (2022) Conjugation in the eukaryotic single-celled organism Euplotes aediculatus (Protozoa, Ciliophora): a focus on nuclear divisions, morphogenesis and pheromones. J King Saud Univ Sci 34:102091

    Article  Google Scholar 

  • Görtz HD (1982) Discharge of cortical ampules in Euplotes aediculatus Pierson, 1943 (Ciliophora, Hypotrichida). Arch Protistenk 125:31–40

    Article  Google Scholar 

  • Grim JN (1967) Ultrastructure of pellicular and ciliary structures of Euplotes eurystomus. J Protozool 14:625–633

    Article  CAS  PubMed  Google Scholar 

  • Grim JN, Halcrow KR, Harshbarger RD (1980) Microtubules beneath the pellicles of two ciliate protozoa as seen with the SEM. J Protozool 27:308–310

    Article  CAS  PubMed  Google Scholar 

  • Gu F, Ji L (1996) An ultrastructural study on cortex and macronucleus of Euplotes encysticus. Zool Res 17:16–22 (in Chinese with English summary)

    Google Scholar 

  • Gu F, Ni B (1993) The exploration of preparing protozoan specimen for scanning electron microscopy. J Chin Electron Microsc Soc 12:525–529

    Google Scholar 

  • Gu F, Ni B (1995) An ultrastructural study on resting cyst of Euplotes encysticus. Acta Biol Exp Sin 28:163–171

    CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Han K, Pan H, Jiang J (2022) Taxonomy and SSU rRNA gene-based phylogeny of two new Euplotes species from China: E. chongmingensis n. sp. and E. paramieti n. sp. (Protista, Ciliophora). BMC Microbiol 22:133

    Article  PubMed  PubMed Central  Google Scholar 

  • Hausmann K, Bradbury PC (1996) Ciliates: cells as organisms. Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Hausmann K, Hausmann E (1981) Structural studies on Trichodina pediculus (Ciliophora, Peritricha): II. The adhesive disc. J Ultrastruct Res 74:144–155

    Article  CAS  PubMed  Google Scholar 

  • Hausmann K, Kaiser J (1979) Arrangement and structure of plates in the cortical alveoli of the hypotrich ciliate, Euplotes vannus. J Ultrastruct Res 67:15–22

    Article  CAS  PubMed  Google Scholar 

  • Hill BE (1981) The cortical morphogenetic cycle associated with cell division in Diophrys Dujardin, 1841 (Ciliophora, Hypotrichida). J Protozool 28:215–221

    Article  Google Scholar 

  • Hill BF, Borror AC (1992) Redefinition of the genera Diophrys and Paradiophrys and establishment of the genus Diophryopsis N. G. (Ciliophora, Hypotrichida): implication for the species problem. J Protozool 39:144–153

    Article  Google Scholar 

  • Hofmann AH, Bardele CF (1987) Stomatogenesis in cyrtophorid ciliates: Trithigmostoma steini (Blochmann, 1895): from somatic Kineties to Oral Kineties. Eur J Protistol 23:2–17

    Article  CAS  PubMed  Google Scholar 

  • Hu X (2008) Cortical structure in non-dividing and dividing Diophrys japonica spec. nov. (Ciliophora, Euplotida) with notes on morphological variation. Eur J Protistol 44:115–129

    Article  PubMed  Google Scholar 

  • Hu X, Huang J, Warren A (2012) The morphology and phylogeny of two euplotid ciliates, Diophrys blakeneyensis spec. nov. and Diophrys oligothrix Borror, 1965 (Protozoa, Ciliophora, Euplotida). Int J Syst Evol Microbiol 62:2757–2773

    Article  PubMed  Google Scholar 

  • Hu X, Lin X, Song W (2019) Ciliate atlas: species found in the South China Sea. Science Press, Beijing

    Google Scholar 

  • Huang J, Dunthorn M, Song W (2012) Expanding character sampling for the molecular phylogeny of euplotid ciliates (Protozoa, Ciliophora) using three markers, with a focus on the family Uronychiidae. Mol Phylogenet Evol 63:598–605

    Article  PubMed  Google Scholar 

  • Huang JB, Zhang T, Zhang Q, Li Y, Warren A, Pan H, Yan Y (2018) Further insights into the highly derived haptorids (Ciliophora, Litostomatea): Phylogeny based on multigene data. Zool Scr 47:231–242

    Article  Google Scholar 

  • Jankowski AW (1978) Revision of a system of class Polyhymenophora (Spirotricha). Tezisy Dokl Zool Inst Akad Nauk SSSR 86:39–40

    Google Scholar 

  • Jankowski AW (1979) Revision of the order Hypotrichida Stein, 1859. Generic catalogue, phylogeny, taxonomy. Trudy Zool Inst Akad Nauk SSSR 86:48–85

    Google Scholar 

  • Jankowski AW (2007) Phylum Ciliophora Doflein, 1901. In: Alimov AF (ed) Protista: Part 2: Handbook on Zoology. Russian Academy of Sciences, Zoological Institute Press, St Petersburg

    Google Scholar 

  • Jiang J, Song W (2010) Two new Diophrys-like genera and their type species, Apodiophrys ovalis n. g., n. sp. and Heterodiophrys zhui n. g., n. sp. (Ciliophora: Euplotida), with notes on their molecular phylogeny. J Eukaryot Microbiol 57:354–361

    Article  PubMed  Google Scholar 

  • Jiang J, Warren A, Song W (2011) Morphology and molecular phylogeny of two new marine euplotids, Pseudodiophrys nigricans n. g., n. sp., and Paradiophrys zhangi n. sp. (Ciliophora: Euplotida). J Eukaryot Microbiol 58:437–445

    Article  PubMed  Google Scholar 

  • Kloetzel JA (1974) Feeding in ciliated protozoa: I. Pharyngeal disks in Euplotes: a source of membrane for food vacuole formation? J Cell Sci 15:379–401

    Article  CAS  PubMed  Google Scholar 

  • Kloetzel JA (1991) Identification and properties of plateins, major proteins in the cortical alveolar plates of Euplotes. J Protozool 38:392–401

    Article  CAS  Google Scholar 

  • Kurth T, Bardele CF (2001) Fine structure of the cyrtophorid ciliate Chlamydodon mnemosyne Ehrenberg, 1837. Acta Protozool 40:33–48

    Google Scholar 

  • Kwon C-B, Lee E-S, Shin M-K (2008) Redescriptions of Diophrys appendiculata and D. scutum (Ciliophora: Spirotrichea: Uronychiidae) new to Korea. Ani Syst Evol Divers 24:191–197

    Article  Google Scholar 

  • Lenzi P, Rosati G (1993) Ultrastructural study of Euplotidium itoi (Ciliata Hypotrichida). Eur J Protistol 29:453–461

    Article  CAS  PubMed  Google Scholar 

  • Li C, Chen X, Zheng W, Doak TG, Fan G, Song W, Yan Y (2021) Chromosome organization and gene expansion in the highly fragmented genome of the ciliate Strombidium stylifer. J Genet Genomics 48:908–916

    Article  CAS  PubMed  Google Scholar 

  • Lian C, Luo X, Warren A, Zhao Y, Jiang J (2020a) Morphology and phylogeny of four marine or brackish water spirotrich ciliates (Protozoa, Ciliophora) from China, with descriptions of two new species. Eur J Protistol 72:125663

    Article  PubMed  Google Scholar 

  • Lian C, Zhang T, Al-Rasheid KA, Yu Y, Jiang J, Huang J (2019) Morphology and SSU rDNA-based phylogeny of two Euplotes species from China: E. wuhanensis sp. n. and E. muscicola Kahl, 1932 (Ciliophora, Euplotida). Eur J Protistol 67:1–14

    Article  PubMed  Google Scholar 

  • Lian C, Wang Y, Li L, Al-Rasheid KA, Jiang J, Song W (2020b) Taxonomy and SSU rDNA-based phylogeny of three new Euplotes species (Protozoa, Ciliophora) from China seas. J King Saud Univ Sci 32:1286–1292

    Article  Google Scholar 

  • Luo X, Hu X, Suzuki T (2014) Microscopic investigation of three species of Diophrys (Ciliophora, Euplotida, Uronychiidae) from Japan, including Diophrys peculiaris nov. spec. Eur J Protistol 50:496–508

    Article  PubMed  Google Scholar 

  • Luporini P, Magagnini G (1970) Recherches sur la structure fine et la biologie reproductive du cilié hypotriche Swedmarkia arenicola Dragesco. Protist 6:113–125

    Google Scholar 

  • Lynn D (2008) The ciliated protozoa: characterization, classification, and guide to the literature, 3rd edn. Springer, Dordrecht

    Google Scholar 

  • Miller MA, Pfeiffer WT, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans, LA

  • Morelli A, Giambelluca A, Lenzi P, Rosati G, Verni F (1996) Ultrastructural features of the peculiar filter-feeding hypotrich ciliate Uronychia transfuga. Micron 27:399–406

    Article  Google Scholar 

  • Nobili R, Rosati-Raffaelli R (1971) The fine structure of the oral apparatus of some oliate hypotrichs. Monit Zool Ital 5:65–80

    Google Scholar 

  • Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, Prjibelski AD, Pyshkin A, Sirotkin A, Sirotkin Y (2013) Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 20:714–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nylander J (2004) MrModeltest V2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University

  • Pan X, Bourland WA, Song W (2013) Protargol synthesis: an in-house protocol. J Eukaryot Microbiol 60:609–614

    Article  CAS  PubMed  Google Scholar 

  • Pitelka DR (1965) New observations on cortical ultrastructure in Paramecium. J Microsc (paris) 4:373–394

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rosati G, Modeo L (2003) Extrusomes in ciliates: diversification, distribution, and phylogenetic implications. J Eukaryot Microbiol 50:383–402

    Article  PubMed  Google Scholar 

  • Rosati G, Verni F, Nobili R, Angeli M (1981) Starvation in Euplotes crassus (Ciliata, Hypotrichida): ultrastructure modifications and effects on reproduction. Acta Protozool 20:225–231

    Google Scholar 

  • Rosati G, Verni F, Bracchi P, Dini F (1987) An ultrastructural analysis of the ciliated protozoon Aspidisca sp. Trans Am Microsc Soc 106:31–52

    Article  Google Scholar 

  • Rosati-Raffaelli G (1970) Fine structure of Diophrys scutum (Dujardin). Arch Anat Microsc Morphol Exp 59:221–234

    CAS  PubMed  Google Scholar 

  • Roth LE (1957) An electron microscope study of the cytology of the protozoan Euplotes patella. J Biophys Biochem Cytol 3:985–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruffolo JJ (1976) Fine structure of the dorsal bristle complex and pellicle of Euplotes. J Morphol 148:469–487

    Article  PubMed  Google Scholar 

  • Serra V, Gammuto L, Nitla V, Castelli M, Lanzoni O, Sassera D, Bandi C, Sandeep BV, Verni F, Modeo L, Petroni G (2020) Morphology, ultrastructure, genomics, and phylogeny of Euplotes vanleeuwenhoeki sp. nov. and its ultra-reduced endosymbiont “Candidatus Pinguicoccus supinus” sp. nov. Sci Rep 10:20311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao C, Zhang Q, Al-Rasheid KA, Warren A, Song W (2010) Ontogenesis and molecular phylogeny of the marine ciliate Diophryopsis hystrix: implications for the systematics of the Diophrys-like species (Ciliophora, Spirotrichea, Euplotida). J Eukaryot Microbiol 57:33–39

    Article  PubMed  Google Scholar 

  • Shen Z, Huang J, Lin X, Yi Z, Li J, Song W (2010) Morphological and molecular characterization of Aspidisca hongkongensis spec. nov. (Ciliophora, Euplotida) from the South China Sea. Eur J Protistol 46:204–211

    Article  PubMed  Google Scholar 

  • Shen Z, Yi Z, Warren A (2011) The morphology, ontogeny, and small subunit rRNA gene sequence analysis of Diophrys parappendiculata n. sp. (Protozoa, Ciliophora, Euplotida), a new marine ciliate from coastal waters of southern China. J Eukaryot Microbiol 58:242–284

    Article  CAS  PubMed  Google Scholar 

  • Sheng Y, Duan L, Cheng T, Qiao Y, Stover NA, Gao S (2020) The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses. Sci China Life Sci 63:1534–1542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi X, Song W, Shi X (1999) Systematic revision of the hypotrichous ciliates. Progress in protozoology. Qingdao Ocean University Press, Qingdao

    Google Scholar 

  • Small EB, Lynn DH (1985) Phylum Ciliophora Doflein 1901. In: Lee J, Hutner SH, Bovee EC (eds) An illustrated guide to the protozoa. Society of Protozoologists, Lawrence, pp 393–575

    Google Scholar 

  • Song W, Packroff G (1993) Beitrag zur morphogenese des marinen ciliaten Diophrys scutum Dujardin, 1841 (Ciliophora, Hypotrichida). Zool Jb Anat 123:85–95

    Google Scholar 

  • Song W, Packroff G (1997) Taxonomische untersuchungen an marinen ciliaten aus China mit beschreibungen von zwei neuen arten, Strombidium globosaneum nov. spec. and S. platum nov. spec. (Protozoa, Ciliophora). Arch Protistenk 147:331–360

    Article  Google Scholar 

  • Song W, Shao C (2017) Ontogenetic patterns of hypotrich ciliates, vol 12. Science Press, Beijing (in Chinese)

    Google Scholar 

  • Song W, Wilbert N (1994) Morphogenesis of the marine ciliate Diophrys oligothrix Borror, 1965 during the cell division (protozoa, ciliophora, hypotrichida). Eur J Protistol 30:38–44

    Article  Google Scholar 

  • Song W, Wilbert N, Chen Z, Shi X (2004) Considerations on the systematic position of Uronychia and related euplotids based on the data of ontogeny and 18S rRNA gene sequence analyses, with morphogenetic redescription of Uronychia setigera Calkins, 1902 (Cilio-phora: Euplotida). Acta Protozool 43:313–328

    CAS  Google Scholar 

  • Song W, Wilbert N, Al-Rasheid K, Warren A, Shao C, Long H, Yi Z, Li L (2007) Redescriptions of two marine hypotrichous ciliates, Diophrys irmgard and D. hystrix (Ciliophora, Euplotida), with a brief revision of the genus Diophrys. J Eukaryot Microbiol 54:283–296

    Article  PubMed  Google Scholar 

  • Song W, Shao C, Yi Z, Li L, Warren A, Al-Rasheid K, Yang J (2009a) The morphology, morphogenesis and SSrRNA gene sequence of a new marine ciliate, Diophrys apoligothrix spec. nov. (Ciliophora; Euplotida). Eur J Protistol 45:38–50

    Article  PubMed  Google Scholar 

  • Song W, Warren A, Hu X (2009b) Free-living ciliates in the Bohai and Yellow Seas. Science Press, Beijing

    Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tuffrau M (1960) Révision du genre Euplotes, fondée sur la comparaison des structures superficielles. Hydrobiologia 15:1–77

    Article  Google Scholar 

  • Tuffrau M (1986) Proposition d’une classification nouvelle de l’ordre Hypotrichida (Protozoa, Ciliophora), fondée sur quelques données récentes. Ann Sci Nat 8:111–117

    Google Scholar 

  • Vďačný P, Foissner W (2017) A huge diversity of metopids (Ciliophora, Armophorea) in soil from the Murray River floodplain, Australia. I. Description of five new species and redescription of Metopus setosus Kahl, 1927. Eur J Protistol 58:35–76

    Article  PubMed  Google Scholar 

  • Wang C, Solberg T, Maurer-Alcalá XX, Swart EC, Gao F, Nowacki M (2022) A small RNA-guided PRC2 complex eliminates DNA as an extreme form of transposon silencing. Cell Rep 40:111263

    Article  CAS  PubMed  Google Scholar 

  • Wicklow BJ (1982a) The Discocephalina (n-subord): Ultrastructure, morphogenesis and evolutionary implications of a group of endemic marine interstitial hypotrichs (Ciliophora, Protozoa). Protist 18:299–330

    Google Scholar 

  • Wicklow BJ (1982b) Morphogenetic and ultrastructural investigation in the Hypotrichida (Ciliophora, Protozoa): implications in ciliate evolution. University of New Hampshire, New Hampshire

    Google Scholar 

  • Wicklow BJ (1983) Ultrastructure and cortical morphogenesis in the euplotine hypotrich Certesia quadrinucleata Fabre-Domergue, 1885 (Ciliophora, Protozoa). J Eukaryot Microbiol 30:256–266

    Google Scholar 

  • Wilbert N (1975) Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos 64:171–179

    Google Scholar 

  • Wu T, Li Y, Lu B, Shen Z, Song W, 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 2:234–348

    Article  Google Scholar 

  • Yang J, Hu X, Shao C, Ma H, Zhu M, Wang M (2008) Morphogenesis of a marine ciliate Diophrys appendiculata (Protozoa, Ciliophora, Euplotida) during cell division. Acta Zool Sin 54:517–524

    Google Scholar 

  • Yi Z, Song W, Clamp JC, Chen Z, Gao S, Zhang Q (2009) Reconsideration of systematic relationships within the order Euplotida (Protista, Ciliophora) using new sequences of the gene coding for small-subunit rRNA and testing the use of combined data sets to construct phylogenies of the Diophrys-complex. Mol Phylogenet Evol 50:599–607

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Huang J, Ye T, Lu B, Chen X (2020a) The morphology and phylogeny of three Diophrys ciliates collected from the subtropical waters of China, including a new species (Ciliophora; Euplotia). J Ocean Univ China 19:975–987

    Article  Google Scholar 

  • Zhang T, Dong J, Cheng T, Duan L, Shao C (2020b) Reconsideration of the taxonomy of the marine ciliate Neobakuella aenigmatica Moon et al., 2019 (Protozoa, Ciliophora, Hypotrichia). Mar Life Sci Technol 2:97–108

    Article  Google Scholar 

  • Zhang T, Li C, Zhang X, Wang C, Roger AJ, Gao F (2021) Characterization and comparative analyses of mitochondrial genomes in single-celled eukaryotes to dhed light on the diversity and evolution of linear molecular architecture. Int J Mol Sci 22:2546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X, Li Y, Duan L, Chen X, Mao F, Juma M, Liu Y, Song W, Gao S (2020) Functional analysis of the methyltransferase SMYD in the single-cell model organism Tetrahymena thermophila. Mar Life Sci Technol 2:109–122

    Article  Google Scholar 

  • Zhao L, Gao F, Gao S, Liang Y, Long H, Lv Z, Su Y, Ye N, Zhang L, Zhao C (2021) Biodiversity-based development and evolution: the emerging research systems in model and non-model organisms. Sci China: Life Sci 64:1236–1280

    Article  PubMed  Google Scholar 

  • Zheng W, Wang C, Lynch M, Gao S (2021) The compact macronuclear genome of the ciliate Halteria grandinella: A transcriptome-like genome with 23,000 nanochromosomes. mBio 20:e01964−01920

  • Zhu C, Bass D, Wang Y, Shen Z, Song W, Yi Z (2020) Environmental parameters and substrate type drive microeukaryotic community structure during short-term experimental colonization in subtropical eutrophic freshwaters. Front Microbiol 11:555795

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32170446, 32030015, 31961123002) and the National Natural Science Foundation of Shanghai (21ZR1419000). The authors would like to express their gratitude to Prof. Weibo Song (Ocean University of China) for his generous help and advice in preparing the manuscript and Dr. Bing Ni (East China Normal University) for his helpful guidance in SEM and TEM. We thank Dr. Tengyue Zhang (Ocean University of China) for providing original cells for this study, and Dr. Tengteng Zhang (Ocean University of China) for her help with the molecular data.

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XP Fan conceptualized the project; JY Dong carried out the research; JY Dong, XP Fan, T Stoeck, YJ Liu, JY Ma and HG Ma helped with data interpretation, wrote, and revised the manuscript. All authors approved the final version of the manuscript.

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Correspondence to Xinpeng Fan.

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Special topic: Ciliatology.

Edited by Jiamei Li.

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Dong, J., Liu, Y., Ma, J. et al. Ultrastructure of Diophrys appendiculata and new systematic consideration of the euplotid family Uronychiidae (Protista, Ciliophora). Mar Life Sci Technol 4, 551–568 (2022). https://doi.org/10.1007/s42995-022-00153-y

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