Linking multi-gene and morphological data in the subclass Scuticociliatia (Protista, Ciliophora) with establishment of the new family Homalogastridae fam. nov.

Mingjian Liu , Limin Jiang , Zhe Zhang , Fan Wei , Honggang Ma , Zigui Chen , Khaled A. S. Al-Rasheid , Hunter N. Hines , Chundi Wang

Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (1) : 1 -22.

PDF
Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (1) :1 -22. DOI: 10.1007/s42995-024-00264-8
Research Paper
research-article
Linking multi-gene and morphological data in the subclass Scuticociliatia (Protista, Ciliophora) with establishment of the new family Homalogastridae fam. nov.
Author information +
History +
PDF

Abstract

Scuticociliatia is one of the most species-rich subclasses in the phylum Ciliophora. The evolutionary relationships among Scuticociliatia groups have long been very unclear due to the homogeneity of morphology and insufficiency of molecular data. With morphological and multi-gene-based molecular data presented here, the evolutionary phylogeny of several Scuticociliatia taxa that were hitherto especially poorly defined is analyzed and discussed. The results indicate: (1) all scuticociliates cluster into two well supported and one poorly supported group, representing three order-level taxa; (2) with the support of both morphological and molecular data, a new family Homalogastridae fam. nov. is proposed in the order Philasterida; (3) Parauronema is formally transferred to Uronematidae and Potomacus is treated as incertae sedis in the order Philasterida, therefore Parauronematidae is proposed to be a junior synonym of Uronematidae; (4) the genus Madsenia and the species Parauronema longum and Pseudocyclidium longum are treated as incertae sedis, while the genus Protophyra should be maintained in the family Ancistridae. In addition, the putative secondary structure of internal transcribed spacer 2 (ITS2) of representative taxa from the three orders of Scuticociliatia are analyzed, and consensus structures and nucleotide composition in each order are exhibited.

Keywords

Ciliated protists / Homalogastridae fam. nov. / Phylogeny / rRNA secondary structure / Scuticociliates

Cite this article

Download citation ▾
Mingjian Liu, Limin Jiang, Zhe Zhang, Fan Wei, Honggang Ma, Zigui Chen, Khaled A. S. Al-Rasheid, Hunter N. Hines, Chundi Wang. Linking multi-gene and morphological data in the subclass Scuticociliatia (Protista, Ciliophora) with establishment of the new family Homalogastridae fam. nov.. Marine Life Science & Technology, 2025, 7(1): 1-22 DOI:10.1007/s42995-024-00264-8

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Antipa GA, Dolan JR, Lynn DH, Obolkina LA, Strüder-Kypke MC. Molecular phylogeny and evolutionary relationships between the ciliate genera Peniculistoma and Mytilophilus (Peniculistomatidae, Pleuronematida). J Eukaryotic Microbiol. 2016, 63: 642-650

[2]

Antipa GA, Strüder-Kypke MC, Lynn DH. Molecular phylogeny, taxonomic relationships and North American distribution of Conchophthirus (Conchophthiridae, Scuticociliatia). Aquat Ecosyst Health Manag. 2020, 23: 58-68

[3]

Bourland W, Pomahač O, Poláková K, Čepička I. Redescription and molecular characterization of Loxocephalus luridus Eberhard, 1862 based on Czech populations: implications for order Loxocephalida Jankowski, 1980. J Eukaryotic Microbiol. 2024, 71 e13028

[4]

Cawthorn R, Lynn D, Despres B, MacMillan R, Maloney R, Loughlin M, Bayer R. Description of Anophryoides haemophila n. sp. (Scuticociliatida: Orchitophryidae), a pathogen of American lobsters Homarus americanus. Dis Aquat Org. 1996, 24: 143-148

[5]

Chi Y, Wei F, Tang D, Mu C, Ma H, Wang Z, Al-Rasheid KAS, Hines HN, Chen X. Exploring the biogeography, morphology, and phylogeny of the condylostomatid ciliates (Alveolata, Ciliophora, Heterotrichea), with establishment of four new Condylostoma species and a revision including redescriptions of five species found in China. Mar Life Sci Technol. 2024, 6: 365-404

[6]

Corliss JO. The ciliated protozoa: characterization, classification and guide to the literature. 19792London, Pergamon Press

[7]

Crooks GE, Hon G, Chandonia J-M, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004, 14: 1188-1190

[8]

Darty K, Denise A, Ponty Y. VARNA: interactive drawing and editing of the RNA secondary structure. Bioinformatics. 2009, 25: 1974-1975

[9]

de Puytorac P. de Puytorac P. Phylum ciliophora doflein, 1901. Traité de Zoologie, Infusoires Ciliés. 1994, Paris, Masson: 115

[10]

Dragesco J, Dragesco-Kernéis A. Ciliés Libres de l’Afrique Intertropicale: Introduction à la Connaissance et à l’étude des Ciliés, Faune Tropicale. 1986, Paris, ORSTOM

[11]

Fenchel T. Ciliates from Scandinavian molluscs. Ophelia. 1965, 2: 71-174

[12]

Foissner W. Das Silberliniensystem von Uronema parduczi sp. n. (Ciliata, Hymenostomatida, Uronematidae). Arch Protistenkd. 1971, 113: 34-50

[13]

Foissner W, Berger H, Kohmann F. Taxonomische und ökologische revision der ciliaten des saprobiensystems—Band III: Hymenostomata, Prostomatida. Nassulida Informationsber Bayer Landesamtes Wasserwirtschaft. 1994, 1(94): 1-548

[14]

Gao F, Katz LA, Song W. Insights into the phylogenetic and taxonomy of philasterid ciliates (Protozoa, Ciliophora, Scuticociliatia) based on analyses of multiple molecular markers. Mol Phylogenet Evol. 2012, 64: 308-317

[15]

Gao F, Strüder-Kypke M, Yi Z, Miao M, Al-Farraj SA, Song W. Phylogenetic analysis and taxonomic distinction of six genera of pathogenic scuticociliates (Protozoa, Ciliophora) inferred from small-subunit rRNA gene sequences. Int J Syst Evol Microbiol. 2012, 62: 246-256

[16]

Gao F, Katz LA, Song W. Multigene-based analyses on evolutionary phylogeny of two controversial ciliate orders: Pleuronematida and Loxocephalida (Protista, Ciliophora, Oligohymenophorea). Mol Phylogenet Evol. 2013, 68: 55-63

[17]

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

[18]

Gao F, Huang J, Zhao Y, Li L, Liu W, Miao M, Zhang Q, Li J, Yi Z, El-Serehy HA, Warren A, Song W. Systematic studies on ciliates (Alveolata, Ciliophora) in China: progress and achievements based on molecular information. Eur J Protistol. 2017, 61: 409-423

[19]

Gong J, Kim S-J, Kim S-Y, Min G-S, Roberts DMcL, Warren A, Choi J-K. Taxonomic redescriptions of two ciliates, Protogastrostyla pulchra n. g., n. comb. and Hemigastrostyla enigmatica (Ciliophora: Spirotrichea, Stichotrichia), with phylogenetic analyses based on 18S and 28S rRNA gene sequences. J Eukaryotic Microbiol. 2007, 54: 468-478

[20]

Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010, 27: 221-224

[21]

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

[22]

Hao T, Song Y, Li B, Pan X. Morphology and molecular phylogeny of three freshwater scuticociliates, with establishments of one new genus and three new species (Ciliophora, Oligohymenophorea). Eur J Protistol. 2022, 86 125918

[23]

Jankowski AW. Parasitic Ciliophora. I. Pectenita golikowi gen. et sp. n. (Entodiscidae fam. n.) from Mizuhopecten yessoensis. Parazitologia. 1973, 7: 214-219

[24]

Jiang L, Wang C, Al-Farraj SA, Hines HN, Hu X. Morphological and molecular examination of the ciliate family Lagynusidae (Protista, Ciliophora, Prostomatea) with descriptions of two new genera and two new species from China. Mar Life Sci Technol. 2023, 5: 178-195

[25]

Kahl A. Neue und wenig bekannte Formen der holotrichen und heterotrichen Ciliaten. Arch Protistenkd. 1926, 55: 197-438

[26]

Kahl A. Die Infusorien (Ciliata) der Oldesloer Salzwasserstellen. Arch Hydrobiol. 1928, 19: 50-123

[27]

Kahl A. Urtiere oder Protozoa. I. Wimpertiere oder Ciliata (Infusoria). 2. Holotricha Tierwelt Dtl. 1931, 21: 181-398

[28]

Kahl A. Grimpe G, Wagler E. Ciliata endocommensalia et parasitica. Die Tierwelt Der Nord Und Ostsee. Lief. 26 (Teil II, C4). 1934, Leipzig, Akademische Verlagsgesellschaft: 147183

[29]

Kofoid CA. On the structure of Protophrya ovicola: a ciliate infusorian from the brood-sac of Littorina rudis Don. Mark Annivers. 1903, 5: 111-120

[30]

Li T, Liu M, Zhang J, Al-Rasheid KAS, Chen Z, Song W, Hines HN, Wang Z. Diversity in freshwater scuticociliates (Alveolata, Ciliophora, Scuticociliatia): two new species isolated from a wetland in northern China, focusing on their morphology, taxonomy, and molecular phylogeny, with establishment of a new family Glauconematidae fam. nov.. Water Biol Secur. 2024, 3: 100275

[31]

Li T, Zhang T, Liu M, Zhang Z, Zhang J, Niu J, Chen X, Al-Farraj SA, Song W. Findings in three endocommensal scuticociliates (Protista, Ciliophora) from freshwater mollusks including morphology and molecular phylogeny with description of two new species. Mar Life Sci Technol. 2024, 6: 212-235

[32]

Liu M, Gao F, Al-Farraj SA, Hu X. Morphology and small subunit rRNA gene sequence of Uronemita parabinucleata n. sp. (Ciliophora, Uronematidae), with an improved generic diagnosis. Eur J Protistol. 2016, 54: 1-10

[33]

Liu M, Li L, Qu Z, Luo X, Al-Farraj SA, Lin X, Hu X. Morphological redescription and SSU rDNA-based phylogeny of two freshwater ciliates, Uronema nigricans and Lembadion lucens (Ciliophora, Oligohymenophorea), with discussion on the taxonomic status of Uronemita sinensis. Acta Protozool. 2017, 56: 17-37

[34]

Liu M, Li L, Zhang T, Fan X, Yi Z, Lin X. Two new scuticociliates from southern China: Uronema apomarinum sp. nov. and Homalogastra parasetosa sp. nov., with improved diagnoses of the genus Homalogastra and its type species Homalogastra setosa (Ciliophora, Oligohymenophorea). Int J Syst Evol Microbiol. 2020, 70: 2405-2419

[35]

Liu M, Wang C, Hu X, Qu Z, Jiang L, Al-Farraj SA, El-Serehy HA, Warren A, Song W (2020b) Taxonomy and molecular phylogeny of three species of scuticociliates from China: Citrithrix smalli gen. nov., sp. nov., Homalogastra binucleata sp. nov. and Uronema orientalis Pan et al., 2015 (Protozoa, Ciliophora, Oligohymenophorea), with the proposal of a new family, Citrithrixidae fam. nov. Front Mar Sci 7:604704

[36]

Liu M, Liu Y, Zhang T, Lu B, Gao F, Gu J, Al-Farraj SA, Hu X, Song W. Integrative studies on the taxonomy and molecular phylogeny of four new Pleuronema species (Protozoa, Ciliophora, Scuticociliatia). Mar Life Sci Technol. 2022, 4: 179-200

[37]

Long H, Song W, Wang Y, Li J. Morphological redescription of two endocommensal ciliates, Entorhipidium fukuii Uyemura, 1934 and Madsenia indomita (Madsen, 1931) Kahl, 1934 from digestive tracts of sea urchins of the Yellow Sea, China (Ciliophora; Scuticociliatida). Eur J Protistol. 2007, 43: 101-114

[38]

Lu B, Hu X, Warren A, Song W, Yan Y. From oral structure to molecular evidence: new insights into the evolutionary phylogeny of the ciliate order Sessilida (Protista, Ciliophora), with the establishment of two new families and new contributions to the poorly studied family Vaginicolidae. Sci China Life Sci. 2023, 66: 1535-1553

[39]

Lynn DH. The ciliated protozoa: characterization, classification, and guide to the literature. 20083Dordrecht, Springer

[40]

Lynn DH, Strüder-Kypke M. Scuticociliate endosymbionts of echinoids (phylum Echinodermata): phylogenetic relationships among species in the genera Entodiscus, Plagiopyliella, Thyrophylax, and Entorhipidium (phylum Ciliophora). J Parasitol. 2005, 91: 1190-1199

[41]

Ma M, Lu B, Fan X, Shi Y, Chen X. Taxonomic clarification of a well-known pathogenic scuticociliate, Miamiensis avidus Thompson & Moewus, 1964 (Ciliophora, Scuticociliatia). J Ocean Univ China. 2018, 17: 1231-1242

[42]

Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey AR, Potter SC, Finn RD, Lopez R. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019, 47: W636-W641

[43]

Magalhães Cardoso PH, de Carvalho Balian S, Reiko Matushima E, Benites de Pádua S, Laterça Martins M (2017) First report of scuticociliatosis caused by Uronema sp. in ornamental reef fish imported into Brazil. Rev Bras Parasitol Vet 26:491–495

[44]

McGowan J, Kilias ES, Alacid E, Lipscombe J, Jenkins BH, Gharbi K, Kaithakottil GG, Macaulay IC, McTaggart S, Warring SD, Richards TA, Hall N, Swarbreck D. Identification of a non-canonical ciliate nuclear genetic code where UAA and UAG code for different amino acids. PLoS Genet. 2023, 19 e1010913

[45]

Miao M, Warren A, Song W, Wang S, Shang H, Chen Z. Analysis of the internal transcribed spacer 2 (ITS2) region of scuticociliates and related taxa (Ciliophora, Oligohymenophorea) to infer their evolution and phylogeny. Protist. 2008, 159: 519-533

[46]

Miller MA, Pfeiffer W, 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, pp 1–8

[47]

Moreira D, von der Heyden S, Bass D, López-García P, Chao E, Cavalier-Smith T. Global eukaryote phylogeny: combined small- and large-subunit ribosomal DNA trees support monophyly of Rhizaria, Retaria and Excavata. Mol Phylogenet Evol. 2007, 44: 255-266

[48]

Nylander JAA. MrModeltest version 2. Evolutionary Biology Centre. 2004, Uppsala, Uppsala University

[49]

Pan X, Yi Z, Li J, Ma H, Al-Farraj SA, Al-Rasheid KAS. Biodiversity of marine scuticociliates (Protozoa, Ciliophora) from China: description of seven morphotypes including a new species, Philaster sinensis spec. nov. Eur J Protistol. 2015, 51: 142-157

[50]

Poláková K, Čepička I, Bourland WA. Phylogenetic position of three well-known ciliates from the controversial order Loxocephalida Jankowski, 1980 (Scuticociliatia, Oligohymenophorea) and Urozona buetschlii (Schewiakoff, 1889) with improved morphological descriptions. Protist. 2021, 172 125833

[51]

Poláková K, Bourland WA, Čepička I. Anaerocyclidiidae fam. nov. (Oligohymenophorea, Scuticociliatia): a newly recognized major lineage of anaerobic ciliates hosting prokaryotic symbionts. Eur J Protistol. 2023, 90: 126009

[52]

Pomp R, Wilbert N. Taxonomic and ecological studies of ciliates from Australian saline soils: colpodids and hymenostomate ciliates. Aust J Mar Freshwater Res. 1988, 39: 479-495

[53]

Qu Z, Weinisch L, Fan X, Katzenmeier S, Stoeck T, Filker S. Morphological, phylogenetic and ecophysiological characterization of a new ciliate, Platynematum rossellomorai n. sp. (Oligohymenophorea, Scuticociliatia), detected in a hypersaline pond on Mallorca, Spain. Protist. 2020, 171: 125751

[54]

Raabe Z. Ordo Thigmotricha (Ciliata-Holotricha) II Familia Hemispeiridae. Acta Protozool. 1970, 7: 117-180

[55]

Rambaut A. FigTree, a graphical viewer of phylogenetic trees (Version 1.4.4). Institute of Evolutionary Biology. 2018, Edinburgh, University of Edinburgh

[56]

Ramsey JM, Brownlee DC, Small EB. Potomacus pottsi Thompson, 1967 (Scuticociliatida, Ciliophora): stomatogenesis with redescription of the microstome trophont. Trans Am Microsc Soc. 1980, 99: 43-51

[57]

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

[58]

Seibel PN, Müller T, Dandekar T, Schultz J, Wolf M. 4SALE—a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinformatics. 2006, 7: 498

[59]

Small EB, Lynn DH. Lee JJ, Hunter SH, Bovee EC. Phylum Ciliophora Doflein, 1901. An illustrated guide to the protozoa. 1985, Lawrence Kansas, Society of Protozoologists: 393-575

[60]

Song W. Morphological studies on the marine pathogenetic ciliate Parauronema longum nov. spec. (Ciliophora, Scuticociliatida). J Ocean Univ Qingdao. 1995, 25: 462-465

[61]

Song W, Wilbert N. Redefinition and redescription of some marine scuticociliates from China, with report of a new species, Metanophrys sinensis nov. spec. (Ciliophora, Scuticociliatida). Zool Anz. 2000, 239: 45-74

[62]

Song W, Zhao Y, Xu K, Hu X, Gong J. Pathogenic protozoa in mariculture. 2003, Beijing (in Chinese), Science Press

[63]

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

[64]

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014, 30: 1312-1313

[65]

Strüder-Kypke MC, Lynn DH. Comparative analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene in ciliates (Alveolata, Ciliophora) and evaluation of its suitability as a biodiversity marker. Syst Biodivers. 2010, 8: 131-148

[66]

Sweeney BA, Hoksza D, Nawrocki EP, Ribas CE, Madeira F, Cannone JJ, Gutell R, Maddala A, Meade CD, Williams LD. R2DT is a framework for predicting and visualising RNA secondary structure using templates. Nat Commun. 2021, 12: 3494

[67]

Thompson JC. Potomacus pottsi n. g., n. sp., a hymenostome ciliate from the Potomac River. J Protozool. 1966, 13: 459-462

[68]

Thompson JC. Parauronema virginianum n. g., n. sp., a marine hymenostome ciliate. J Protozool. 1967, 14: 731-734

[69]

Wang Z, Chi Y, Li T, Song W, Wang Y, Wu T, Zhang G, Liu Y, Ma H, Song W, Al-Rasheid KAS, Warren A, Lu B. Biodiversity of freshwater ciliates (Protista, Ciliophora) in the Lake Weishan Wetland, China: the state of the art. Mar Life Sci Technol. 2022, 4: 429-451

[70]

Wang Z, Feng X, Li L, Al-Rasheid KAS, Warren A, Wang C, Gu Z. New considerations on the phylogeny of Sessilida (Protista: Ciliophora: Peritrichia) based on multiple-gene information, with emphasis on colonial taxa. Mar Life Sci Technol. 2022, 4: 569-583

[71]

Wu T, Cheng T, Cao X, Jiang Y, Al-Rasheid KAS, Warren A, Wang Z, Lu B. On four epibiotic peritrichous ciliates (Protozoa, Ciliophora) found in Lake Weishan Wetland: morphological and molecular data support the establishment of a new genus, Parapiosoma gen. nov., and two new species. Mar Life Sci Technol. 2023, 5: 337-358

[72]

Xie J, Chen Y, Cai G, Cai R, Hu Z, Wang H (2023) Tree visualization by one table (tvBOT): a web application for visualizing, modifying and annotating phylogenetic trees. Nucleic Acids Res 51:W587–W592

[73]

Xu K, Song W. Morphological studies on a commensal ciliate, Pseudocyclidium longum nov. spec. (Ciliophora, Scuticociliatida) of the mantle cavity of marine mollusc Cyclina sinensis (Gmelin, 1791) from the coast of the Yellow Sea. Yellow Sea. 1998, 4: 1-4

[74]

Yi Z, Song W, Clamp JC, Chen Z, Gao S, Zhang Q. 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. 2009, 50: 599-607

[75]

Zhang T, Vďačný P. Re-discovery and novel contributions to morphology and multigene phylogeny of Myxophyllum steenstrupi (Ciliophora: Pleuronematida), an obligate symbiont of terrestrial pulmonates. Zool J Linn Soc. 2021, 192: 1-23

[76]

Zhang T, Vďačný P. Re-discovery and novel contributions to morphology and multigene phylogeny of Protospirella mazurica (Raabe, 1968) Aescht, 2001 (Ciliophora: Pleuronematida), an obligate symbiont of the river nerite Theodoxus fluviatilis Linnaeus, 1758 (Mollusca: Gastropoda). Eur J Protistol. 2023, 88 125956

[77]

Zhang T, Vďačný P. Deciphering phylogenetic relationships of and delimiting species boundaries within the controversial ciliate genus Conchophthirus using an integrative morpho-evo approach. Mol Phylogenet Evol. 2024, 190 107931

[78]

Zhang T, Fan X, Gao F, Al-Farraj SA, El-Serehy HA, Song W. Further analyses on the phylogeny of the subclass Scuticociliatia (Protozoa, Ciliophora) based on both nuclear and mitochondrial data. Mol Phylogenet Evol. 2019, 139 106565

[79]

Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31: 3406-3415

RIGHTS & PERMISSIONS

The Author(s)

PDF

309

Accesses

0

Citation

Detail

Sections
Recommended

/