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Light microscopy observations on the encystation and excystation processes of the ciliate Phacodinium metchnikoffi (Ciliophora, Phacodiniidae), including additional information on its resting cysts structure

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Abstract

The scope of our study presents a light microscopy study on the encystation, excystation and morphology of the resting cysts of the spirotrich ciliate, Phacodinium metchnikoffi. During the encystation process, the trophic cell changes in shape, size and volume, the horseshoe-shaped macronuclear nodule transforms into a compact rounded mass, the ciliature is resorbed and the cyst wall is formed. A characteristic accumulation of dark substances in the cell cytoplasm was observed. The most significant feature is the surface. Ornamentation in the form of protuberances in regular rows is located on the entire surface of the cysts. We also focused on the excystation process for the first time and uncovered several specifics of P. metchnikoffi excystation. The excystation is characterised by the formation of the excystation vacuole. An escape apparatus is also present. The coexistence of the excystation vacuole and apparatus during the excystation process is an unusual type of escaping and has not yet been described. The results suggest that not only the resting cysts surface, but also the excystation and encystation processes are much more varied than literary data indicate.

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References

  • Akematsu T, Matsuoka T (2007) Excystment-inducing factors in the ciliated protozoan Colpoda cucullus: hydrophobic peptides are involved in excystment induction. Acta Protozool 46:9–14

    CAS  Google Scholar 

  • Barrero SS (2010) Characterización filogenética de Phacodinium metchnikoffi: Análisis comparativo de datos morfológicos, morfogenéticos y moleculares. Universidad Comlutense de Madrid

  • Beers CD (1945) The excystation process in the ciliate Didinium nasutum. J Elisha Mitchell Sci Soc 61:264–275

    Google Scholar 

  • Beers CD (1948) Excystation in the ciliate Bursaria truncatella. Biol Bull 94:86–98. https://doi.org/10.2307/1538347

    Article  PubMed  CAS  Google Scholar 

  • Beers CD (1966) The excystation process in the ciliate Nassula ornata Ehrbg. J Protozool 13:79–83. https://doi.org/10.1111/j.1550-7408.1966.tb01874.x

    Article  PubMed  CAS  Google Scholar 

  • Benčaťová S, Tirjaková E (2017a) Prvonález druhu Bresslauides terricola (Foissner, 1987) Foissner, 1993 (Ciliophora, Colpodea) na Slovensku – cystické štádiá, en- a excystácia. Folia Faun Slovaca 22:31–40

    Google Scholar 

  • Benčaťová S, Tirjaková E (2017b) A study on resting cysts of an oxytrichid soil ciliate, Rigidohymena quadrinucleata (Dragesco and Njine, 1971) Berger, 2011 (Ciliophora, Hypotrichia), including notes on its encystation and excystation process. Acta Protozool 56:77–91

    Google Scholar 

  • Benčaťová S, Tirjaková E, Vďačný P (2016) Resting cysts of Parentocirrus hortualis Voss, 1997 (Ciliophora, Hypotrichia), with preliminary notes on encystation and various types of excystation. Eur J Protistol 43:295–314. https://doi.org/10.1016/j.ejop.2015.12.003

    Google Scholar 

  • Berger H (1999) Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monogr Biol 78:1–1080. https://doi.org/10.1007/978-94-011-4637-1

    Google Scholar 

  • Calvo P, Torres A, Navas P, Perez-Silva J (1983) Complex carbohydrates in the cyst wall of Histriculus similis. J Gen Microbiol 129:829–832. https://doi.org/10.1099/00221287-129-3-829

    CAS  Google Scholar 

  • Cavaleiro J, Fernandes NM, da Silva-Neto ID, Soares CAG (2017) Resting cysts of the pigmented ciliate Blepharisma sinuosum Sawaya, 1940 (Ciliophora: Heterotrichea). J Eukarytic Microbiol. https://doi.org/10.1111/jeu.12483

  • Certes A (1891) Note sur deux infusoires nouveaux des environs de Paris. Mém Soc Zool France 4:536–541

    Google Scholar 

  • da Silva-Neto ID (1993) Structural and ultrastructural observations of the ciliate Phacodinium metchnikoffi certes, 1891 (Heterotrichea, Phacodiniida). Eur J Protistol 29:209–218

    Article  PubMed  Google Scholar 

  • Didier P, Dragesco J (1979a) Organisation ultrastructurale du cortex de Phacodinium metchnikoffi (cilié hétérotriche). Protist 15:33–42

    Google Scholar 

  • Didier P, Dragesco J (1979b) Organisation ultrastructurale du cortex des vacuoles digestives de Phacodinium metchnikoffi (cilié hétérotriche). Trans Am Microsc Soc 98:385–392. https://doi.org/10.2307/3225723

    Article  Google Scholar 

  • Dragesco J (1970) Ciliés libres du Cameroun. Num Hors-Série Ann Fac Sci Yaoundé:1–141

  • Fernández-Galiano D, Calvo P (1992) Redescription of Phacodinium metchnikoffi (Ciliophora, Hypotrichida): general morphology and taxonomic position. J Protozool 39:443–448. https://doi.org/10.1111/j.1550-7408.1992.tb04829.x

    Article  PubMed  Google Scholar 

  • Foissner W (1993) Colpodea (Ciliophora). PRO 4:1–798

    Google Scholar 

  • Foissner W (2009) The stunning, glass-covered resting cyst of Maryna umbrellata (Ciliophora, Colpodea). Acta Protozool 48:223–242

    PubMed  PubMed Central  CAS  Google Scholar 

  • Foissner I, Foissner W (1987) The fine structure of the resting cysts of Kahliella simplex (Ciliata, Hypotrichida). Zool Anz 218:65–74

    Google Scholar 

  • Foissner W, Stoeck T (2009) Morphological and molecular characterization of a new protist family Sandmanniellidae n. Fam. (Ciliophora, Colpodea), with description of Sandmaniella terricola n. G., n. Sp. from the Chobe floodplain in Botswana. J Eukaryot Microbiol 56:472–483

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Foissner W, Müller H, Agatha S (2007) A comparative fine structural and phylogenetic analysis of resting cysts in oligotrich and hypotrich Spirotrichea (Ciliophora). Eur J Protistol 43:295–314. https://doi.org/10.1016/j.ejop.2007.06.001

    Article  PubMed  PubMed Central  Google Scholar 

  • Funadani R, Suetomo Y, Matsuoka T (2013) Emergence of the terrestrial ciliate Colpoda cucullus from a resting cyst: rupture of the cyst wall by active expansion of an excystation vacuole. Microbes Environ 28:149–152. https://doi.org/10.1264/jsme2.ME12145

    Article  PubMed  Google Scholar 

  • Funadani R, Sogame Y, Kojima K, Takeshita T, Yamamota K, Tsujizono T, Suizu F, Miyata S, Yagyu KI, Suzuki T, Arikawa M, Matsuoka T (2016) Morphogenetic and molecular analyses of cyst wall components in the ciliated protozoan Colpoda cucullus Nag-1. FEMS microbial Lett 363: fnw203. https://doi.org/10.1093/femsle/fnw203

  • Grecco N, Bussers JC (1990) Ultrastructural localization of chitin in the cystic wall of Euplotes muscicola Kahl (Ciliata, Hypotrichidia). Eur J Protistol 26:75–80. https://doi.org/10.1016/S0932-4739(11)80390-1

    Article  Google Scholar 

  • Grimes GW, Hammersmith RL (1980) Analysis of the effects of encystment and excystment on incomplete doublets of Oxytricha fallax. J Embryol Exp Morpholog 59:19–26

    CAS  Google Scholar 

  • Gutiérrez JC, Callejas S, Borniquel S, Benítez L, Martín-González A (2001) Ciliate cryptobiosis: a microbial strategy against an eviromental starvation. Int Microbiol 4:151–157. https://doi.org/10.1007/s10123-001-0030-3

    PubMed  Google Scholar 

  • Gutiérrez JC, Diáz S, Ortega R, Martín-González A (2003) Ciliate resting cyst walls: a comparative review. Recent Res Dev Microbiol 7:361–379

    Google Scholar 

  • Kahl A (1932) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria). In: Dahl, F. (de.), Die Tierwelt Deutschlands, G. Fisher, Jena

  • Kim Y, Taniguchi A (1995) Excystation of the oligotrich ciliate Strombidium conicum. Aquat Microb Ecol 9:149–156. https://doi.org/10.3354/ame009149

    Article  Google Scholar 

  • Klionsky DJ, Emr SD (2000) Cell biology - autophagy as a regulated pathway of cellular degradation. Science 290:1717–1721

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Levy MR, Elliott AM (1968) Biochemical and ultrastructural changes in Tetrahymena pyriformis during starvation. J Protozool 15:208–222. https://doi.org/10.1111/j.1550-7408.1968.tb02113.x

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Sun Q, Fan X, Wu N, Ni B, Gu F (2017) The differentiation of cellular structure during encystment in the soil hypotrichous ciliate Australocirrus cf. australis (Protista, Ciliophora). Anim Cells Syst 21:45–52. https://doi.org/10.1080/19768354.2016.1262896

    Article  CAS  Google Scholar 

  • Liu Z, Yi-Song L, Jun-Gang L, Fu-Kang G (2009) Some ultrastructural observations of the vegetative, resting and excysting ciliate, Urostyla grandis (Urostylidae, Hypotrichida). Biol Res 42:395–401

    PubMed  Google Scholar 

  • Lynn DH (2008) The ciliated protoza: characterization, classification, and guide to the literature. Springer, Canada

    Google Scholar 

  • Martín-González A, Benítez A, Gutiérrez JC (1992) Ultrastructural analysis of resting cysts and encystment in Colpoda inflata. 2. Encystment process and a review of ciliate resting cyst classification. Cytobios 72:93–106

    Google Scholar 

  • Matsusaka T (1979) Effect of cycloheximide on the encystment and ultrastructure of the ciliate, Histriculus. J Protozool 26:619–625. https://doi.org/10.1111/j.1550-7408.1979.tb04208.x

    Article  CAS  Google Scholar 

  • Montagnes DJS, Lowe CD, Poulton A, Jonsson P (2002) Redescription of Strombidium oculatum Gruber 1884 (Ciliophora, Oligotrichia). J Eukaryot Microbiol 49:329–337. https://doi.org/10.1111/j.1550-7408.2002.tb00379.x

    Article  PubMed  Google Scholar 

  • Müller H (2007) Live observation of excystation in the spirotrich ciliate Meseres corlissi. Eur J Protistol 43:95–100. https://doi.org/10.1016/j.ejop.2006.11.003

    Article  PubMed  Google Scholar 

  • Penard E (1922) Etudes sur les Infusoires d’eau douce. Georg et Cie, Genève. https://doi.org/10.5962/bhl.title.6785

  • Prowazek S (1899-1903) Protozoenstudien I.III. Zoologischen Instituten der Universität Wien, pp 11-14

  • Rawlinson NG, Gates MA (1985) The excystment process in the ciliate Euplotes muscicola: an integrated light and scanning electron microscopic study. J Protozool 32:729–735. https://doi.org/10.1111/j.1550-7408.1985.tb03109.x

    Article  Google Scholar 

  • Reid PC, John AWG (1983) Resting cysts in the ciliate class Polyhymenophorea: phylogenetic implications. J Protozool 30:710–713. https://doi.org/10.1111/j.1550-7408.1983.tb05348.x

    Article  Google Scholar 

  • Repak AJ (1968) Encystment and excystation of the heterotrichous ciliate Blepharisma stoltei Isquith. J Protozool 15:407–412. https://doi.org/10.1111/j.1550-7408.1968.tb02148.x

    Article  Google Scholar 

  • Roque M (1970) Observations Sur Phacodinium metchnikoffi certes, 1891. Ann Stat Biol Besse-en-Chandesse 5:297–302

    Google Scholar 

  • Shin MK, Hwang UW, Kim W, Wright ADG, Krawczyk C, Lynn DH (2000) Phylogenetic position of the ciliates Phacodinium (order Phacodiniida) and Protocruzia (subclass Protocruziidia) and systematics of the spirotrich ciliates examined by small subunit ribosomal RNA gene sequences. Eur J Protistol 36:293–302. https://doi.org/10.1016/S0932-4739(00)80005-X

    Article  Google Scholar 

  • Tsutsumi S, Watoh T, Kumamoto K, Kotsuki H, Matsuoka T (2004) Effects of porphyrins on encystment and excystment in ciliated protozoan Colpoda sp. Jpn J Protozool 37:119–126

    Google Scholar 

  • Vďačný P, Foissner W (2012) Monograph of the dileptids (Protista, Ciliophora, Rhynchostomatia). Denisia 31:1–529

    Google Scholar 

  • Verni F, Rosati G (2011) Resting cysts: A survival strategy in Protozoa Ciliophora. Ital. J. Zool. 78: 134–145. https://doi.org/10.1080/11250003.2011.560579

  • Walker GK, Maugel TK, Goode D (1975) Some ultrastructural observations on encystment in Stylonychia mytilus (Ciliophora: Hypotrichida). Trans Am Microsc Soc 94:147–154. https://doi.org/10.2307/3225545

    Article  Google Scholar 

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Acknowledgements

This work was supported by the Slovak Scientific Grant Agency (Project No. 1/0114/16 and Project No. 1/0041/17). We would also like to thank RNDr. Viktória Čabanová for collecting the moss samples and Mike Sabo for English correction.

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  1. Department of Zoology, Faculty of Natural Sciences, Comenius University in Bratislava, Ilkovičova 6, Mlynská dolina B-1, 842 15, Bratislava, Slovak Republic

    Simona Benčaťová & Eva Tirjaková

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  1. Simona Benčaťová
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  2. Eva Tirjaková
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Correspondence to Simona Benčaťová.

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Benčaťová, S., Tirjaková, E. Light microscopy observations on the encystation and excystation processes of the ciliate Phacodinium metchnikoffi (Ciliophora, Phacodiniidae), including additional information on its resting cysts structure. Biologia 73, 467–476 (2018). https://doi.org/10.2478/s11756-018-0059-9

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