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Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954: a unique hypotrichid ciliate having a highly specialized developmental pattern during binary division

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Abstract

In sharp contrast to their pelagic relatives, the oligotrichs, the overwhelming majority of hypotrich ciliates inhabit the benthos. Only a few species, including those of the genus Hypotrichidium Ilowaisky, 1921, have adapted to a planktonic lifestyle. The ontogenetic mode of the highly differentiated ciliate, Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954, is unknown. In this study, the interphase morphology and the ontogenetic process of this species are investigated. Accordingly, the previously unidentified ciliary pattern of Hypotrichidium is redefined. The main morphogenetic features are as follows: (1) The parental adoral zone of membranelles is inherited completely by the proter and the oral primordium of the opisthe arises in a deep pouch. (2) Five frontoventral cirral anlagen (FVA) are formed: FVA I contributes to the single frontal cirrus, FVA II–IV generate three frontoventral cirral rows, FVA V migrates and forms postoral ventral cirri. (3) All marginal cirral row anlagen develop de novo: each of the two left anlagen forms a single cirral row, while the single right anlage fragments into anterior and posterior parts. (4) Two dorsal kinety anlagen occur de novo, with the right one fragmenting to form kineties 2 and 3. (5) Two long caudal cirral rows are formed at the ends of dorsal kineties 1 and 3. On the basis of the morphogenetic features and phylogenetic analyses, the assignment of Hypotrichidium to the family Spirofilidae Gelei, 1929 within Postoralida is supported. The establishment of separate families for the slender “tubicolous” spirofilids and the highly helical spirofilids is also validated.

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Data availability

The small subunit ribosomal RNA gene sequences generated during the present study have been deposited to GenBank with accession number: ON117314–ON117316 (https://www.ncbi.nlm.nih.gov/nuccore). The other data generated or analyzed during this study are included in this manuscript and supporting files.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 31900319, 32030015, 32070432), the National Key Research and Development Program of China (No. 2018YFD0900701), and the Youth Innovation Promotion Association of the Chinese Academy of Sciences (No. 2019333). We thank Prof. Xiaozhong Hu, Ocean University of China (OUC), for his helpful suggestions regarding species identification, and Prof. Weibo Song, OUC, for his comments on the manuscript.

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  1. Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Xiaotian Luo & Jie Huang

  2. Institute of Evolution and Marine Biodiversity & Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, China

    Honggang Ma & Yujie Liu

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

    Xiaoteng Lu

  4. Department of Zoology, Faculty of Science, Charles University, Prague, 12843, Czech Republic

    William A. Bourland

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Contributions

W.A.B: conceived and guided the study. X.Luo: collected samples and carried out the laboratory work. X.Lu: was responsible for the molecular phylogenetic analyses. X.Luo: drafted the manuscript. J.H, H.M, Y.L, X.Lu, and W.A.B: made further revisions. All authors read and approved the final version of manuscript

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Edited by Jiamei Li.

Special topic: Ciliatology.

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42995_2022_148_MOESM1_ESM.doc

Supplementary file1 Supplementary Fig. S1 A–L Photomicrographs showing interphase (A) and morphogenetic stages (B–J) of Hypotrichidium tisiae after protargol staining. A Ventral view of a typical specimen, showing infraciliature, arrowhead shows the single frontal cirrus, arrow indicates the acutely pointed tail. B Details of a very early divider, showing the replication bands of the macronuclear nodules (arrows), arrowheads mark the micronuclei. C Oral primordium of the opisthe. D Ventral view of an early divider, showing the V-shaped frontoventral cirral anlage and the right marginal cirral row anlage. E Ventral view of an early-middle divider, showing the elongated frontoventral cirral anlagen and the left marginal cirral row anlagen. F Details of an early-middle divider, showing five streak-like frontoventral cirral anlagen in the opisthe, arrow indicates the newly formed adoral membranelles. G The oral primordium located in the deep pouch (arrowhead) and the micronucleus. H Ventral view of a middle divider, showing new cirri formed from cirral anlagen, arrowhead indicates the newly formed frontal cirrus. I Dorsal view of a middle divider, showing dorsal kinety anlagen and caudal cirral row analgen. J Dorsal view of a middle-late divider, arrowhead shows the gap between anterior and posterior parts of the right marginal cirral row, arrows indicate caudal cirral row 2 fragmented from the end of dorsal kinety 3. ARMR new anterior part of right marginal cirral row, CC1, 2A caudal cirral row anlage, DK2, 3 new dorsal kineties, DK1–3A dorsal kinety anlagen, FVR1–3 new frontoventral cirral rows, LM1A left marginal cirral row 1 anlage, Mi micronuclei, OP oral primordium, PRMR new posterior part of right marginal cirral row, PVC new postoral ventral cirri, RMA right marginal cirral row anlage, I–V frontoventral cirral anlagen. Scale bar: 50 μm (DOC 2764 KB)

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Luo, X., Huang, J., Ma, H. et al. Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954: a unique hypotrichid ciliate having a highly specialized developmental pattern during binary division. Mar Life Sci Technol 4, 536–550 (2022). https://doi.org/10.1007/s42995-022-00148-9

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