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Doublets of the unicellular organism Euplotes vannus (Alveolata, Ciliophora, Euplotida): the morphogenetic patterns of the ciliary and nuclear apparatuses associated with cell division

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Abstract

Ciliated protists are one of the most diverse and highly differentiated group among unicellular organisms. Doublets occur in ciliates when two cells fuse into a single individual. Doublets contain two major cellular components (either cell in a doublet) and have traditionally been considered as developmental anomalies. Nevertheless, doublets can divide or even conjugate effectively, which may represent dispersal forms of the life stages. In addition, morphogenesis, as an important process in the life cycle, will provide important insights into the complex differentiation mechanism and various physiological phenomena. However, morphogenetic studies focusing on doublets of ciliates are very limited, which has become an obstacle to understand their complete life history. Here we isolated a doublet strain from the marine species Euplotes vannus (Müller, 1786) Diesing, 1850 and investigated its morphogenetic events during asexual reproduction. Our results indicate that: (1) the opisthe’s oral primordium develops de novo beneath the cortex; (2) the frontoventral and transverse cirral anlagen, cirrus I/1, and marginal anlagen in both dividers develop de novo separately; (3) the dorsal kinety anlagen, the three rightmost ones of which produce three caudal cirri for the proter, occur within the parental structures in the mid-body region; (4) the opisthe acquires two caudal cirri, one from the end of each two rightmost kineties; and (5) there are two macronuclei and one micronucleus in the doublet and they divide amitotically and mitotically, respectively. Finally, we speculate that this special differentiation may be an adaptive form to adverse environments.

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The authors declare that all data supporting the findings of this study are available within the article.

References

  • Abello A, Régnier V, Arnaiz O, Le Bars R, Bétermier M, Bischerour J (2020) Functional diversification of Paramecium Ku80 paralogs safeguards genome integrity during precise programmed DNA elimination. PLoS Genet 16:e1008723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asghar U, Chi Y, Gao YY, Lu BR, Jiang YH, Gong RT, Ma HG, Al-Rasheid KAS, Gao F (2021) Morphogenesis of the ciliature during sexual process of conjugation in the ciliated protist Euplotes raikovi. Front Mar Sci 7:615377

    Article  Google Scholar 

  • Bell AJ, Satir P, Grimes GW (2008) Mirror-imaged doublets of Tetmemena pustulata: implications for the development of left–right asymmetry. Dev Biol 314:150–160

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Jiang YH, Gao F, Zheng WB, Krock TJ, Stover NA, Lu C, Katz LA, Song WB (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 

  • Dawson JA (1920) An experimental study of an amicronucleate Oxytricha. II. the formation of double animals or ‘twins.’ J Exp Zool 30:129–158

    Article  Google Scholar 

  • Dias RJP, Paiva TS, Silva-Neto ID, D’Agosto M (2007) Description of a mirror-image doublet from a Brazilian strain of Gastrostyla setifera (Engelmann, 1862) Kent, 1882 (Ciliophora: Stichotrichia). Eur J Protistol 43:179–184

    Article  PubMed  Google Scholar 

  • Duan L, Cheng T, Wei F, Qiao Y, Wang C, Warren A, Niu J, Wang YY (2021) New contribution to epigenetic studies: isolation of micronuclei with high purity and DNA integrity in the model ciliated protist Tetrahymena thermophila. Eur J Protistol 80:125804

    Article  PubMed  Google Scholar 

  • Fenchel T (2004) Orientation in two dimensions: chemosensory motile behaviour of Euplotes vannus. Eur J Protistol 40:49–55

    Article  Google Scholar 

  • Gao YY, Gong RT, Jiang YH, Pan B, Li Y, Warren A, Jiang JM, 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 

  • Grimes GW (1982) Pattern determination in hypotrich ciliates. Am Zool 22:35–46

    Article  Google Scholar 

  • Gruber DF, Tuorto S, Taghon GL (2009) Growth phase and elemental stoichiometry of bacterial prey influences ciliate grazing selectivity. J Eukaryot Microbiol 56:466–471

    Article  CAS  PubMed  Google Scholar 

  • He W, Shi XB (1990) Studies on buccal neighbouring mirror-image doublet in Stylonychia mytilus. Nat Sci J Harbin Norm Univ 6:78–85

    Google Scholar 

  • Jerka-Dziadosz M (1983) The origin of mirror-image symmetry doublet cells in the hypotrich ciliate Paraurostyla weissei. Rouxs Arch Dev Biol 192:179–188

    Article  Google Scholar 

  • Jerka-Dziadosz M (1985) Mirror-image configuration of the cortical pattern causes modifications in propagation of microtubular structures in the hypotrich ciliate Paraurostyla weissei. Rouxs Arch Dev Biol 194:311–324

    Article  Google Scholar 

  • Jiang JM, Shao C, Xu HL, Al-Rasheid KAS (2010) Morphogenetic observations on the marine ciliate Euplotes vannus during cell division (Protozoa: Ciliophora). J Mar Biol Assoc UK 90:683–689

    Article  Google Scholar 

  • Jiang YH, Zhang TT, Vallesi A, Yang XY, Gao F (2019) Time-course analysis of nuclear events during conjugation in the marine ciliate Euplotes vannus and comparison with other ciliates (Protozoa, Ciliophora). Cell Cycle 18:288–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimball RF (1941) Double animals and amicronucleate animals in Euplotes patella with particular reference to their conjugation. J Exp Zool 86:1–33

    Article  Google Scholar 

  • Kosaka T (1990) Conjugation between unimicronuclear doublets and singlets, and several features of the clones originating from hemikarya of Euplotes woodruffi syngen 1 (Ciliophora). Eur J Protistol 26:65–74

    Article  CAS  PubMed  Google Scholar 

  • Li L, Qiu ZJ, Chen Y, Sun YJ (2004) Experiment of transposition between different regions in mirror-image doublets of Stylonychia mytilus (Protozoa: Ciliophora: Hypotrichida). Acta Zool Sin 50:808–816

    Google Scholar 

  • Lian CY, Luo XT, Warren A, Zhao Y, Jiang JM (2020) 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 

  • Liu WW, Shin MK, Yi ZZ, Tan YH (2021) Progress in studies on the diversity and distribution of planktonic ciliates (Protista, Ciliophora) in the South China Sea. Mar Life Sci Technol 3:28–43

    Article  CAS  Google Scholar 

  • Luporini P, Giachetti C (1980) Multiconjugant complexes of Euplotes crassus: an instance of coordination of nuclear events. J Protozool 27:108–112

    Article  Google Scholar 

  • Luporini P, Bracchi P, Esposito F (1979) Specific contact-dependent cell-to-cell communication during preconjugant interactions of the ciliate Euplotes crassus. J Cell Sci 39:201–213

    Article  CAS  PubMed  Google Scholar 

  • Miceli C, Luporini P (1982) Experimental evidence for effective heterokaryon formation in the ciliate Euplotes crassus. J Exp Zool 222:17–26

    Article  Google Scholar 

  • Miyake A (1974) Cell interaction in conjugation of ciliates. Curr Top Microbiol Immunol 64:49–77

    CAS  PubMed  Google Scholar 

  • Munyenyembe K, Timmons C, Weiner AKM, Katz LA, Yan Y (2021) DAPI staining and DNA content estimation of nuclei in uncultivable microbial eukaryotes (Arcellinida and ciliates). Eur J Protistol 81:125840

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pan YB, Zhang WJ, Lin SJ (2018) Transcriptomic and microRNAomic profiling reveals molecular mechanisms to cope with silver nanoparticle exposure in the ciliate Euplotes vannus. Environ Sci Nano 5:2921–2935

    Article  CAS  Google Scholar 

  • Powers EL (1943) The mating types of double animals in Euplotes patella. Am Midl Nat 30:175–195

    Article  Google Scholar 

  • Ricci N, Banchetti R, Pelamatti R (1989) Reversible carnivory in Oxytricha bifaria: a peculiar ecological adaptation. Hydrobiologia 182:115–120

    Article  Google Scholar 

  • Ricci N, Erra F, Banchetti R (2000) The behavior of the doublet of Oxytricha bifaria (Ciliata, Hypotrichida): a contribution to the understanding of this enigmatic form. J Eukaryot Microbiol 47:156–160

    Article  CAS  PubMed  Google Scholar 

  • Serra V, Fokin SI, Gammuto L, Nitla V, Castelli M, Basuri CK, Satyaveni A, Sandeep BV, Modeo L, Petroni G (2021) Phylogeny of Neobursaridium reshapes the systematics of Paramecium (Oligohymenophorea, Ciliophora). Zool Scr 50:241–268

    Article  Google Scholar 

  • Sheng YL, He M, Zhao FQ, Shao C, Miao M (2018) Phylogenetic relationship analyses of complicated class Spirotrichea based on transcriptomes from three diverse microbial eukaryotes: Uroleptopsis citrina, Euplotes vannus and Protocruzia tuzeti. Mol Phylogenet Evol 129:338–345

    Article  PubMed  Google Scholar 

  • Shi XB, Frankel J (1990) Morphology and development of mirror-image doublets of Stylonychia mytilus. J Protozool 37:1–13

    Article  CAS  PubMed  Google Scholar 

  • Shi XB, Qiu ZJ (1989) Induction of amicronucleate mirror-imaged doublet in the ciliate Stylonychia mytilus and observation on its reproductive behavior. Acta Zool Sin 35:364–369

    Google Scholar 

  • Song WB, Packroff G (1997) Taxonomische Untersuchungen an marinen Ciliaten aus China mit Beschreibungen von 2 neuen Arten, Strombidium globosaneum nov. spec. und Strombidium platum nov. spec. (Protozoa, Ciliophora). Arch Protistenk 147:331–360

    Article  Google Scholar 

  • Tang DX, Wang XY, Dong JY, Li Y, Gao F, Xie HB, Zhao CT (2020) Morpholino-mediated knockdown of ciliary genes in Euplotes vannus, a novel marine ciliated model organism. Front Microbiol 11:549781

    Article  PubMed  PubMed Central  Google Scholar 

  • Tchang TR, Pang YB (1965) Condition for the artificial induction of monster jumelles of Stylonychia mytilus which are capable of reproduction. Sci Sin 14:1331–1338

    Google Scholar 

  • Tchang TR, Pang YB (1980) Ciliature and genetic dynamics of jumelle Stylonychia mytilus. Sci China 11:1099–1104 (in Chinese with English summary)

    Google Scholar 

  • Vd’ačný P, Tirjaková E (2012) Taxonomic revision and neotypification of Zosterodasys transversus (Kahl, 1928), with description of a mirror-image doublet (Ciliophora, Phyllopharyngea, Synhymeniida). Acta Protozool 51:39–54

    Google Scholar 

  • Wang JY, Zhang TT, Li FC, Warren A, Li YB, Shao C (2021) A new hypotrich ciliate, Oxytricha xianica sp. nov., with notes on the morphology and phylogeny of a Chinese population of Oxytricha auripunctata Blatterer & Foissner, 1988 (Ciliophora, Oxytrichidae). Mar Life Sci Technol 3:303–312

    Article  CAS  Google Scholar 

  • Wang CD, Solberg T, Maurer-Alcalá XX, Swart CE, 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 

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

    Google Scholar 

  • Xu KD, Foissner W (2005) Morphology, ontogenesis and encystment of a soil ciliate (Ciliophora, Haptorida), Arcuospathidium cultriforme (Penard, 1922), with models for the formation of the oral bulge, the ciliary patterns, and the evolution of the spathidiids. Protistology 4:5–55

    Google Scholar 

  • Yano J, Suhama M (1991) Pattern formation in mirror-image doublets of the ciliate Stylonychia pustulata. J Protozool 38:111–121

    Article  Google Scholar 

  • Zhang TY, Dong JY, Cheng T, Duan LL, Shao C (2020) 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 X, Lu XT, Chi Y, Jang YH, Wang CD, Al-Farraj SA, Vallesi A, Gao F (2022) Timing and characteristics of nuclear events during conjugation and genomic exclusion in Paramecium multimicronucleatum. Mar Life Sci Technol 4:317–328

    Article  CAS  Google Scholar 

  • Zhao L, Gao F, Gao S, Liang YJ, Long HA, Lv ZY, Su Y, Ye NH, Zhang LS, Zhao CT, Wang XY, Song WB, Zhang SC, Dong B (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 WB, Wang CD, Lynch M, Gao S (2021) The compact macronuclear genome of the ciliate Halteria grandinella: a transcriptome-like genome with 23,000 nanochromosomes. mBio 12:e0196420

    Article  Google Scholar 

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Acknowledgements

Our special thanks are given to Prof. Weibo Song (OUC) for his kind suggestions during drafting of the manuscript. This work was supported by the National Natural Science Foundation of China (32030015, 31922013 and 31961123002), the Natural Science Foundation of Shandong Province (ZR2020JQ13), the Fundamental Research Funds for the Central Universities (202141004), and the Researchers Supporting Project (RSP-2022R7) of the King Saud University, Saudi Arabia.

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Author notes

  1. Jinyu Fu and Yong Chi contributed equally to this work.

Authors and Affiliations

  1. Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, 266003, China

    Jinyu Fu, Yong Chi & Feng Gao

  2. Department of Biology, Shenzhen MSU-BIT University, Shenzhen, 518172, China

    Xiaoteng Lu

  3. Zoology Department, College of Science, King Saud University, Riyadh, 11451, Saudi Arabia

    Saleh A. Al-Farraj

  4. Department of Biology, University of Pisa, 56126, Pisa, Italy

    Giulio Petroni

  5. Engineering Research Center of Environmental DNA and Ecological Water Health Assessment, Shanghai Ocean University, Shanghai, 201306, China

    Jiamei Jiang

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  1. Jinyu Fu
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Contributions

FG and JJ were responsible for the conceptualization and supervision of the study. JF performed cell culture and staining. YC performed live observations. JF, YC, GP and JJ contributed to the revision of the manuscript. All authors contributed to the article and approved the submitted version.

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Correspondence to Jiamei Jiang.

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Edited by Jiamei Li.

Special topic: Ciliatology.

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Fu, J., Chi, Y., Lu, X. et al. Doublets of the unicellular organism Euplotes vannus (Alveolata, Ciliophora, Euplotida): the morphogenetic patterns of the ciliary and nuclear apparatuses associated with cell division. Mar Life Sci Technol 4, 527–535 (2022). https://doi.org/10.1007/s42995-022-00150-1

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