Abstract
Marine ciliates from Japan were insufficiently studied. In this work, three species of class Spirotrichea Bütschli, 1889, collected from coastal water of Nagasaki, were morphologically investigated using protargol staining method. The results revealed that one represents an unknown species, Caryotricha orientalis nov. spec., and the others can be identified as Paradiophrys irmgard (Mansfeld, 1923) Jankowski, 1978 and Actinotricha saltans Cohn, 1866, the latter two species being new records for Japan. The new species is characterized by its medium-sized body, 19 adoral membranelles, about eight cirral rows extending posteriorly to mid-body, six transverse cirri arranged in two rows, and a migratory row of four cirri as well as eight dorsal kineties. Meanwhile, supplementary data on morphology and micrographs and ecological factors were provided for two known species, which thus help to circumscribe both species and increase our knowledge about distribution.
References
- Bai, Y., Wang, R., Song, W., Li, L., Santoferrara, L. & Hu, X. (2020) Three redescriptions in Tintinnopsis (Protista: Ciliophora: Tintinnina) from coastal waters of China, with cytology and phylogenetic analyses based on ribosomal RNA genes. BMC Microbiology, 20, 374. https://doi.org/10.1186/s12866-020-02057-2
- Berger, H. (1999) Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biologicae, 78, 1–1080. https://doi.org/10.1007/978-94-011-4637-1_1
- Bharti, D. & Kumar, S. (2023) Description of a new oxytrichid ciliate, Oxytricha buxai n. sp. and redescription of O. quadricirrata Blatterer and Foissner, 1988 based on morphology and 18S rDNA analyses. European Journal of Protistology, 88, 125959. https://doi.org/10.1016/j.ejop.2023.125959
- Borror, A. (1972) Revision of the order Hypotrichida (Ciliophora, Protozoa). Journal of Protozoology, 19, 1–23. https://doi.org/10.1111/j.1550-7408.1972.tb03407.x
- Dragesco, J. (1963) Compléments à la connaissance des ciliés mésopsammiques de Roscoff. II. Heterotriches III. Cahiers de Biologie Marine, 4, 251–275.
- Fan, Y., Chen, X., Hu, X., Shao, C., Al-Rasheid, K., Al-Farraj, S. & Lin, X. (2014a) Morphology and morphogenesis of Apoholosticha sinica n. g., n. sp. (Ciliophora, Hypotrichia), with consideration of its systematic position among urostylids. European Journal of Protistology, 50, 78–88. https://doi.org/10.1016/j.ejop.2013.06.003
- Fan, Y., Pan, Y., Huang, J., Lin, X., Hu, X. & Warren, A. (2014b) Molecular phylogeny and taxonomy of two novel brackish water hypotrich ciliates, with the establishment of a new genus, Antiokeronopsis gen. n. (Ciliophora, Hypotrichia). Journal of Eukaryotic Microbiology, 61, 449–462. https://doi.org/10.1111/jeu.12125
- Fan, Y., Warren, A., Al-Farraj, S.A., 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). Journal of Morphology, 274, 395–403. https://doi.org/10.1002/jmor.20097
- Feng, X., Méndez-Sánchez, D., Zhuang, W., Li, R., Pomahač, O., Čepička, I., Rotterová, J. & Hu, X. (2024a) Morphology, morphogenesis, and molecular characterization of Castula specialis sp. nov. (Ciliophora, Armophorea, Metopida). Journal of Eukaryotic Microbiology, 71, e13014. https://doi.org/10.1111/jeu.13014
- Feng, X., Zhuang, W., Li, R. & Hu, X. (2024b) Ontogeny and phylogeny of the anaerobic genus Urostomides with supplementing morphological characterization of the type and one little known species (Alveolata, Ciliophora, Armophorea). Zoological Journal of the Linnean Society, zlae055. https://doi.org/10.1093/zoolinnean/zlae055
- Fotedar, R., Stoeck, T., Filker, S., Fell, J., Agatha, S., Marria, 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. Journal of Eukaryotic Microbiology, 63, 578–590. https://doi.org/10.1111/jeu.12305
- Ghaffar, A., Bai, Y. & Hu, X. (2023) First record of two urotsylid ciliates (Protozoa: Ciliophora: Spirotrichea) from Japan expanding the circumscription of species. Journal of Natural History, 57, 724–743. https://doi.org/10.1080/00222933.2023.2206586
- Hada, Y. (1932) The Tintinnoinea from the Sea of Okhotsk and its neighborhood. Journal of the Faculty of Science, Hokkaido University Series 6 Zoolology, 2, 37–59.
- Hartwig, E. (1973) Die Ciliaten des Gezeiten-Sandstrandes der Nordseeinsel Sylt. I. Systematik. Akademie der Wisenschaften und der Literatur, Mainz. Mathematisch-Naturwissenschaftliche Klasse Mikrofauna Meersbodens, 18, 387–453.
- Hill, B.F. & Borror, A.C. (1992) Redefinition of the genera Diophrys and Paradiophrys and establishment of the genus Diophryopsis n. g. (Ciliophora, Hypotrichida): Implication for the species problem. Journal of Protozoology, 39, 144–153. https://doi.org/10.1111/j.1550-7408.1992.tb01294.x
- Hu, X. (2008) Cortical structure in non-dividing and dividing Diophrys japonica spec. nov. (Ciliophora, Euplotida) with notes on morphological variation. European Journal of Protistology, 44, 115–129. https://doi.org/10.1016/j.ejop.2007.08.007
- Hu, X. & Suzuki, T. (2004) A new species of Holosticha (Ciliophora: Hypotrichida) from the coastal waters of Nagasaki, Japan: Holosticha nagasakiensis sp. nov. Journal of the Marine Biological Association of the United Kingdom, 84, 9–13. https://doi.org/10.1017/S0025315404008847h
- Hu, X. & Suzuki, T. (2005) Light microscopical observations on two marine dysteriid ciliates from Japan, including a description of Dysteria yagiui nov. spec (Ciliophora, Cyrtophorida). European Journal of Protistology, 41, 29–36. https://doi.org/10.1017/S0025315404008847h
- Hu, X., Fan, Y. & Warren, A. (2015) New record of Apoholosticha sinica (Ciliophora, Urostylida) from the UK: morphology, 18S rRNA gene phylogeny and notes on morphogenesis. International Journal of Systematic and Evolutionary Microbiology, 65, 2549–2561. https://doi.org/10.1099/ijs.0.000301
- Hu, X, Lin, X. & Song, W. (2019) Ciliate atlas: Species found in the South China Sea. Science Press, Beijing, 631 pp. https://doi.org/10.1007/978-981-13-5901-9
- Hu, X, Warren, A. & Suzuki, T. (2004) Morphology and morphogenesis of two marine ciliates, Pseudokeronopsis pararubra sp. n. and Amphisiella annulata from China and Japan (Protozoa: Ciliophora). Acta Protozoologica, 43, 351–368.
- Jankowski, A.W. (1978) Systematic revision of the class Polyhymenophora (Spirotricha), morphology, systematics and evolution, and phylogeny of the order Hypotrichida Stein, 1859 (Protozoa, Ciliophora). Tezisy Doklady Zoologiche Instituta Akademi Nauk SSSR, 86, 39–40 (in Russian).
- 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). Journal of Eukaryotic Microbiology, 58, 437–445. https://doi.org/10.1111/j.1550-7408.2011.00567.x
- Jiang, J., Xing, Y., Miao, M., Shao, C., Warren, A. & Song, W. (2013) Two new marine ciliates, Caryotricha rariseta n. sp. and Discocephalus pararotatorius n. sp. (Ciliophora, Spirotrichea), with phylogenetic analyses inferred from the small-subunit rRNA gene sequences. Journal of Eukaryotic Microbiology, 60, 388–398. https://doi.org/10.1111/jeu.12046
- Jiang, L., Wang, C., Al-Farraj, S., Hines, H. & Hu, X. (2023) Morphological and molecular examination of the ciliate family Lagynusidae (Protista, Ciliophora, Prostomatea) and descriptions of two new genera and two new species from China. Marine Life Science & Technology, 5, 178–195. https://doi.org/10.1007/s42995-023-00174-1
- Jiang, L., Wang, C., Liao, L., Al-Farraj, S., Warren, A. & Hu, X. (2024) Re-evaluation of the systematic position of the order Prostomatida (Protista: Ciliophora), with the establishment of two new genera and two new species. Zoological Journal of the Linnean Society, 200, 849–864. https://doi.org/10.1093/zoolinnean/zlad116
- Jiang, L., Wang, C., Warren, A., Ma, H. & Hu, X. (2022) New considerations on the systematics of the family Holophryidae (Protozoa, Ciliophora, Prostomatea), with a description of Holophrya paradiscolor sp. nov. and a redescription of Pelagothrix plancticola. Systematics and Biodiversity, 20, 1–15. https://doi.org/10.1080/14772000.2021.2012296
- Kahl, A. (1932) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 3. Spirotricha. Tierwelt Deutschlands, 25, 399–650.
- Kouser, F., Liao, L. & Hu, X. (2024) Morphology and molecular phylogeny of a Chinese population of Rubrioxytricha guamensis Kumar et al., 2018 (Ciliophora, Hypotrichia). Journal of Natural History, 58, 688–701. https://doi.org/10.1080/00222933.2024.2361963
- Kouser, F, Song, W., Jiang, L., Zhuang, W., Wang, C., Wu, T. & Hu, X. (2022) Taxonomy and phylogeny of two spirotrichean ciliates (Alveolata, Protista, and Ciliophora) from a plateau saline–alkaline lake in Tibet, China, including description of a new species. Frontiers in Marine Science, 9, 836341. https://doi.org/10.3389/fmars.2022.836341
- Kumar, S., Bharti, D., Kabir, A.S., Hong, J.S., Shin, M.K. (2018) Rubrioxytricha guamensis nov. spec. (Ciliophora, Spirotricha), a novel hypotrich ciliate from Guam (United States), Micronesia. Journal of Eukaryotic Microbiology, 65, 392–399. https://doi.org/10.1111/jeu.12484
- Küppers, G. (2020) A new species of Uronychia (Spirotrichea: Euplotida) from Argentina. European Journal of Protistology, 75, 125706. https://doi.org/10.1016/j.ejop.2020.125706
- Li, J., Zhan, Z. & Xu, K. (2017) Systematics and molecular phylogeny of the ciliate genus Pseudokeronopsis (Ciliophora, Hypotrichia). Journal of Eukaryotic Microbiology, 64, 850–872. https://doi.org/10.1111/jeu.12420
- Li, R., Zhuang, W., Feng, X., Al-Farraj, S.A., Schrecengost, A., Rotterová, J., Beinart, R. & Hu, X. (2023) Molecular phylogeny and taxonomy of three anaerobic plagiopyleans (Alveolata: Ciliophora), retrieved from two geographically distant localities in Asia and North America. Zoological Journal of the Linnean Society, 199, 493−510. https://doi.org/10.1093/zoolinnean/zlad015
- Li, R., Zhuang, W., Feng, X., Al-Farraj, S.A., Warren, A., Hu, X. (2022) Phylogeny of the anaerobic ciliate genus Sonderia (Protista: Ciliophora: Plagiopylea), including the description of three novel species and a brief revision of the genus. Marine Life Science & Technology, 4, 493−512. https://doi.org/10.1007/s42995-022-00142-1
- Li, R., Zhuang, W., Feng, X., Zhu, X. & Hu, X. (2024) Morphology and molecular phylogeny of three Parasonderia species including a new species (Ciliophora, Plagiopylea). European Journal of Protistology, 94, 126087. https://doi.org/10.1016/j.ejop.2024.126087
- Lian, C., Luo, X., Warren, A., Zhao, Y. & Jiang, J. (2020) Morphology and phylogeny of four marine or brackish water spirotrich ciliates (Protozoa, Ciliophora) from China, with descriptions of two new species. European Journal of Protistology, 72, 125663. https://doi.org/10.1016/j.ejop.2019.125663
- Liao, L., Jiang, L. & Hu, X. (2024) Integrative data of a novel ciliate (Alveolata, Ciliophora) propose the establishment of Heterodeviata nantongensis nov. sp. BMC Microbiology, 24, 27. https://doi.org/10.1186/s12866-024-03190-y
- Lu, X., Gao, F., Shao, C., Hu, X. & Warren, A. (2014) Morphology, morphogenesis and molecular phylogeny of a new marine ciliate, Trichototaxis marina n. sp. (Ciliophora, Urostylida). European Journal of Protistology, 50, 524–537. https://doi.org/10.1016/j.ejop.2014.08.002
- Luo, X., Hu, X. & Suzuki, T. (2014) Microscopic investigation on three species of Diophrys (Ciliophora, Euplotida, Uronychiidae) from Japan, including Diophrys peculiaris nov. spec. European Journal of Protistology, 50, 496–508. https://doi.org/10.1016/j.ejop.2014.08.003
- Lynn, D.H. (2008) The ciliated protozoa: Characterization, classification, and guide to the literature. Third edition. Springer, Dordrecht, 605 pp.
- Mansfeld, K. (1923) 16 neue oder wenig bekannte marine Infusorien. Archiv für Protistenkunde, 46, 97–140.
- Miao, M., Shao, C., Jiang, J., Li, L., Stoeck, T. & Song, W. (2009) Caryotricha minuta (Xu et al., 2008) nov. comb., a unique marine ciliate (Protista, Ciliophora, Spirotrichea) with phylogenetic estimation of the ambiguous genus Caryotricha inferred from small subunit rDNA sequence. International Journal of Systematic and Evolutionary Microbiology, 59, 430–438. https://doi.org/10.1111/jeu.12753
- Moon, J.H., Kim, J.H., Quintela-Alonso, P. & Jung, J.H. (2020) Morphology, morphogenesis, and molecular phylogeny of Neobakuella aenigmatica n. sp. (Ciliophora, Spirotrichea, Bakuellidae). Journal of Eukaryotic Microbiology, 67, 54–65. https://doi.org/10.1111/jeu.12753
- Omar, A., Moon, J.H., Nam, S.W. & Jung, J.H. (2021) Tunicothrix halophila n. sp., a secondarily oligomerized parabirojimid hypotrich (Ciliophora, Spirotrichea) from hypersaline coastal water in Korea. Frontiers in Microbiology, 12, 691361. https://doi.org/10.3389/fmicb.2021.691361
- Omar, A., Choi, J.H. & Jung, J.H. (2023a) New record of ten ciliate species (Protozoa, Ciliophora) from South Korea. Journal of Species Research, 12, 95–108.
- Omar, A., Jang, S.W. & Jung, J.H. (2023b) Polymorphism, gigantism, and cannibalism, one stylonychid ciliate (Ciliophora, Hypotricha) to rule them all. Frontiers in Microbiology, 14, 1159634. https://doi.org/10.3389/fmicb.2023.1159634
- Omar, A., Yeo, J.H. & Jung, J.H. (2022) A new “flagship” ciliate, Pseudostylonychia obliquocaudata n. gen., n. sp. (Ciliophora, Hypotricha), from South Korea. European Journal of Protistology, 84, 125893. https://doi.org/10.1016/j.ejop.2022.125893
- Ozaki, Y. & Yagiu, R. (1943) Studies on the marine ciliates of Japan, mainly the Setonaikai (the Inland Sea of Japan), I. Journal of Science of the Hiroshima University Series B, Division 1, 10, 21–52.
- Park, K.M., Jung, J.H. & Min, G.S. (2013) Morphology, morphogenesis, and molecular phylogeny of Anteholosticha multicirrata n. sp. (Ciliophora, Spirotrichea) with a note on morphogenesis of A. pulchra (Kahl, 1932) Berger, 2003. Journal of Eukaryotic Microbiology, 60, 564–577. https://doi.org/10.1111/jeu.12060
- Rees, J.van (1884) Protozen der Oosterschelde (Protozoaires de l'escaut de I'est). Tijdschr. ned. dierk. Ver een., Supplement Deel I (years 1883/1884), 592–673. [in Dutch]
- Shao C., Song, W., Al-Rasheid, K.A.S. & Berger, H. (2011) Redefinition and reassignment of the 18-cirri genera Hemigastrostyla, Oxytricha, Urosomoida, and Actinotricha (Ciliophora, Hypotricha), and description of one new Genus and two new species. Acta Protozoolgica, 50, 263–287.
- Song, W., Shin, M.K. & Kim, W. (1991) Morphology and infraciliature of the marine ciliate Oxytricha saltans (Cohn, 1866) Kahl, 1932 (Protozoa, Ciliophora, Hypotrichida). The Korean Journal of Systematic Zoology, 7, 233–240.
- Song, W., Warren, A. & Hu, X. (2009) Free-living ciliates in the Bohai and Yellow Seas, China. Science Press, Beijing, 518 pp.
- Song, W. & Wilbert, N. (1997) Morphological investigations on some free living ciliates (Protozoa, Ciliophora) from China Sea with description of a new hypotrichous genus, Hemigastrostyla nov. gen. Archiv für Protistenkunde, 148, 413–444. https://doi.org/10.1016/S0003-9365(97)80020-6
- Song, W., Wilbert, N., Al-Rasheid, K.A.S., 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. Journal of Eukaryotic Microbiology, 54, 283–296. https://doi.org/10.1111/j.1550-7408.2007.00266.x
- Tang, Q., Shao, C., Jin, D., Warren, A., Wang, J. & Li, J. (2022) Morphology, cell division, and phylogeny of Notohymena antartica Foissner, 1996 and Engelmanniella mobilis (Engelmann, 1862) Foissner, 1982 (Ciliophora, Hypotrichia). European Journal of Protistology, 84, 125879. https://doi.org/10.1016/j.ejop.2022.125879
- Vd’acňý, P. & Foissner, W. (2021) Morphology and ontogenesis of two new Hemiholosticha species (Ciliophora, Hypotrichia, Hemiholostichidae nov. fam.). European Journal of Protistology, 77, 125763. https://doi.org/10.1016/j.ejop.2020.125763
- Wang, C., Hu, Y., Warren, A. & Hu, X. (2021a) Genetic diversity and phylogeny of the genus Euplotes (Protozoa, Ciliophora) revealed by the mitochondrial CO1 and nuclear ribosomal genes. Microorganisms, 9, 2204. https://doi.org/10.3390/microorganisms9112204
- Wang, C., Jiang, L., Liao, L., Qu, Z., Kumar, S. & Hu, X. (2023a) Taxonomic and phylogenetic studies on two marine cyrtophorians (Protista: Ciliophora: Phyllopharyngea) with the establishment of a new species. Systematics and Biodiversity, 21, 2269150. https://doi.org/10.1080/14772000.2023.2269150
- Wang, C., Jiang, L., Pan, H., Warren, A. & Hu, X. (2023b) New contributions to the Cyrtophoria ciliates (Protista, Ciliophora): Establishment of new taxa and phylogenetic analyses using two ribosomal genes. Journal of Eukaryotic Microbiology, 70, e12938. https://doi.org/10.1111/jeu.12938
- Wang, R., Bai, Y., Hu, T., Xu, D., Suzuki, T. & Hu, X. (2021b) Integrative taxonomy and molecular phylogeny of three poorly known tintinnine ciliates, with the establishment of a new genus (Protista; Ciliophora; Oligotrichea). BMC Ecology and Evolution, 21, 115. https://doi.org/10.1186/s12862-021-01831-8
- Wang, Y., Wang, J., Wang, B., Wang, K. & Shao, C. (2023) Morphological, ontogenetic, and phylogenetic research of a poorly known non-dorsomaginalian ciliate: Erniella filiformis Foissner, 1987 (Protist, Ciliophora, Hypotricha). European Journal of Protistology, 91, 126031. https://doi.org/10.1016/j.ejop.2023.126031
- Wanick, R.C. & Silva-Neto, I.D. da. (2004) Benthic ciliates from Sepetiba Bay (Rio de Janeiro, Brazil) with description of Pseudokeronopsis sepetibensis n. sp. (Spirotrichea: Urostylida). Zootaxa, 587, 1–11. https://doi.org/10.11646/zootaxa.587.1.1
- Wilbert, N. (1975) Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos, 64, 171–179. [in German]
- Xu, K., Lei, Y. & Choi, J.K. (2008) Kiitricha minuta n. sp., a peculiar hypotrichous ciliate (Ciliophora, Spirotrichea) from the Yellow Sea. Journal of Eukaryotic Microbiology, 55, 201–206. https://doi.org/10.1111/j.1550-7408.2008.00313.x
- Xu, W., Ma, J., Li, Y., Bourland, W., Petroni, G., Luo, X. & Song, W. (2022) Phylogeny of a new ciliate family Clampidae fam. nov. (Protista: Ciliophora), with notes on morphology and morphogenesis. Zoological Journal of the Linnean Society, 196, 88–104. https://doi.org/10.1093/zoolinnean/zlab102
- Zhang, T., Wang, J., Lyu, Z., Wang, Y., Al-Rasheid, K.A,S. & Shao, C. (2022) Morphology, morphogenesis and phylogeny of a new soil ciliate, Bistichella sinensis n. sp., and morphology of two oxytrichids (Ciliophora, Hypotrichia). European Journal of Protistology, 86, 125934. https://doi.org/10.1016/j.ejop.2022.125934
- Zhuang, W., Li, R. Feng, X., Al-Farraj, S.A. & Hu, X. (2022) New contribution to the diversity of the anaerobic genus Metopus (Ciliophora, Armophorea), with descriptions of three new marine species. Frontiers in Marine Science, 9, 884834. https://doi.org/10.3389/fmars.2022.884834
- Živaljic, S., Scherwass, A., Schoenle, A., Hohlfeld, M., Quintela-Alonso, P., Nitsche, F. & Arndt, H. (2020) A barotolerant ciliate isolated from the abyssal deep sea of the North Atlantic: Euplotes dominicanus sp. n. (Ciliophora, Euplotia). European Journal of Protistology, 73, 125664. https://doi.org/10.1016/j.ejop.2019.125664