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Acta Protozoologica

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Future prospects for investigating ciliate biodiversity

Publication date: 2022

Acta Protozoologica, 2022, Volume 61, pp. 35 - 46

https://doi.org/10.4467/16890027AP.22.005.16236

Authors

,
Ľubomír Rajter
Phycology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany
Eukaryotic Microbiology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany
All publications →
,
Borong Lu
Institute of Evolution and Marine Biodiversity & College of Fisheries, Ocean University of China, Qingdao, China
All publications →
,
Erika Rassoshanska
Eukaryotic Microbiology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany
All publications →
Micah Dunthorn
Natural History Museum, University of Oslo, Oslo, Norway
Eukaryotic Microbiology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany
All publications →

Abstract

Ciliates have a long history of being central in evolutionary and ecological studies on eukaryotic microorganisms. Although thousands of species have been discovered, their total diversity still remains unknown. Here, we will discuss two unsolved problems that hinder the further exploration of ciliate diversity at the species level, and potential solutions to these problems are proposed. First, ciliate morphospecies are difficult to identify because the different silver stains are not scalable (they do not represent high-throughput methods) and basic supplies are lacking (e.g., protargol); a solution may be the development of fluorescent staining techniques. Second, ciliate phylogenetic species are difficult to identify because of extensive paralogy in nuclear-protein-coding genes; a solution may be to concentrate on sequencing mitochondrial genomes. These two approaches could be integrated into a high-throughput fluorescent-single-cell sorting and mitochondrial genomes sequencing process that would enable the observation and better understanding of ciliate species on a massive scale.

References

Abal M., Souto A. A., Amat-Guerri F., Acuña A. U., Andreu, J. M., Barasoain I. (2001) Centrosome and spindle pole microtubules are main targets of a fluorescent taxoid inducing cell death: centrosome impairment by fluorescent taxoid. Cell Motil. Cytoskel. 49: 1–15

Abraham J. S., Sripoorna S., Maurya S., Makhija S., Gupta R., Toteja R. (2019) Techniques and tools for species identification in ciliates: a review. Int. J. Syst. Evol. Microbiol. 69: 877–894

Acosta-Mercado D., Lynn, D. H. (2003) The edaphic quantitative protargol stain: a sampling protocol for assessing soil ciliate abundance and diversity. J. Microbiol. Methods 53: 365–375

Adl S. M., Leander B. S., Simpson A. G. B., Archibald J. M., Anderson O. R., Bass D., Bowser S. S., Brugerolle G., Farmer M. A., Karpov S., Kolisko M., Lane C. E., Lodge D. J., Mann D. G., Meisterfeld R., Mendoza L., Moestrup Ø., Mozley-Standridge S. E., Smirnov, A. V., Spiegel F. (2007) Diversity,  nomenclature, and taxonomy of protists. Syst. Biol. 56: 684–689

Aescht E. (2008) Annotated catalogue of “type material”of ciliates (Ciliophora) and some further protists at the Upper Austrian Museum in Linz, including a guideline for “typification”of species. Denisia 23: 125–234

Aescht E. (2001) Catalogue of the generic names of ciliates (Protozoa, Ciliophora). Denisia 1: 1–350

Albert T. J., Molla M. N., Muzny D. M., Nazareth L., Wheeler D., Song X., Richmond T. A., Middle C. M., Rodesch M. J., Packard C. J., Weinstock G. M., Gibbs R. A. (2007). Direct selection of human genomic loci by microarray hybridization. Nat. Methods 4: 903–905

Allen S. L., Li C. I. (1974) Nucleotide sequence divergence among DNA fractions of different syngens of Tetrahymena pyriformis. Biochem. Genet. 12: 213–233

Arregui L., Muñoz-Fontela C., Guinea A., Serrano S. (2003) FLUTAX facilitates visualization of the ciliature of oxytrichid hypotrichs. Eur. J. Protistol. 39: 169–172

Arregui L., Muñoz-Fontela C., Serrano S., Barasoain I., Guinea A. (2002) Direct Visualization of the Microtubular Cytoskeleton of Ciliated Protozoa with a Fluorescent Taxoid. J. Eukaryot. Microbiol. 49: 312–318

Aubusson-Fleury A., Balavoine G., Lemullois M., Bouhouche K., Beisson J., Koll F. (2017) Centrin diversity and basal body patterning across evolution: new insights from Paramecium. Biol. Open 6: 765–776

Aubusson-Fleury A., Bricheux G., Damaj R., Lemullois M., Coffee G., Donnadieu F., Koll F., Viguès B., Bouchard P. (2013) Epiplasmins and epiplasm in Paramecium: the building of a submembraneous cytoskeleton. Protist 164: 451–469

Aubusson-Fleury A., Cohen J., Lemullois M. (2015) Ciliary heterogeneity within a single cell: the Paramecium model. Methods Cell Biol. 127: 457–485

Aubusson-Fleury A., Lemullois M., de Loubresse N. G., Laligné C., Cohen J., Rosnet O., Jerka-Dziadosz M., Beisson J., Koll F. (2012) The conserved centrosomal protein FOR20 is required for assembly of the transition zone and basal body docking at the cell surface. J. Cell Sci. 125: 4395–4404

Augustin H., Foissner W., Adam H. (1984) An improved pyridinated silver carbonate method which needs few specimens and yields permanent slides of impregnated ciliates (Protozoa, Ciliophora). Mikroskopie. 41: 134–137

Aury J. M., Jaillon O., Duret L., Noel B., Jubin C., Porcel B. M., Ségurens B., Daubin V., Anthouard V., Aiach N., Arnaiz O., Billaut A., Beisson J., Blanc I., Bouhouche K., Câmara F., Duharcourt S., Guigo R., Gogendeau D., Katinka M., Keller A. M., Kissmehl R., Klotz C., Koll F., Le Mouël A., Lepère G., Malinsky S., Nowacki M., Nowak J. K., Plattner H., Poulain J., Ruiz F., Serrano V., Zagulski M., Dessen P., Bétermier M., Weissenbach J., Scarpelli C., Schächter V., Sperling L., Meyer E., Cohen J., Wincker P. (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444: 171–178

Barasoain I., Díaz J. F., Andreu J. M. (2010) Fluorescent taxoid probes for microtubule research. Methods Cell Biol. 95: 353–372

Barth D., Berendonk T. U. (2011) The mitochondrial genome sequence of the ciliate Paramecium caudatum reveals a shift in nucleotide composition and codon usage within the genus Paramecium. BMC Genomics 12: 272

Barth D., Krenek S., Fokin S. I., Berendonk T. U. (2006) Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. J. Eukaryot. Microbiol. 53: 20–25

Beisson J., Bétermier M., Bré M. H., Cohen J., Duharcourt S., Duret L., Kung C., Malinsky S., Meyer E., Preer J. R., Sperling L. (2010) Immunocytochemistry of Paramecium cytoskeletal structures. Cold Spring Harb. Protoc. 2010, pdb.prot5365

Beisson J., Clérot J. C., Fleury-Aubusson A., de Loubresse N. G., Ruiz F., Klotz C. (2001) Basal body-associated nucleation center for the centrin-based cortical cytoskeletal network in Paramecium. Protist 152: 339–354

Boscaro V., Rossi A., Vannini C., Verni F., Fokin S. I., Petroni G. (2017) Strengths and biases of high-throughput sequencing data in the characterization of freshwater ciliate microbiomes. Microb. Ecol. 73: 865–875

Brunk C. F., Kahn R. W., Sadler L. A. (1990) Phylogenetic relationships among Tetrahymena species determined using the polymerase chain reaction. J. Mol. Evol. 30: 290–297

Callen A.-M., Adoutte A., Andrew J. M., Baroin-Tourancheau A., Bré M.-H., Ruiz P. C., Clérot J.-C., Delgado P., Fleury A., Jeanmaire-Wolf R., Viklicky V., Villalobo E., Levilliers N. (1994) Isolation and characterization of libraries of monoclonal antibodies directed against various forms of tubulin in Paramecium. Biol. Cell 81: 95–119

Canals O., Obiol A., Muhovic I., Vaqué D., Massana R. (2020) Ciliate diversity and distribution across horizontal and vertical scales in the open ocean. Mol. Ecol. 29: 2824–2839

Chatton E., Lwoff A. (1930) Imprégnation, par diffusion argentique, de l’infraciliature des ciliés marins et d’eau douce, après fixation cytologique et sans dessication. C. R. Soc. Biol. 104: 834–836

Chen X., Zhao X., Liu X., Warren A., Zhao F., Miao, M. (2015) Phylogenomics of non-model ciliates based on transcriptomic analyses. Protein Cell 6: 373–385

Clamp J. C., Lynn D. H. (2017) Investigating the biodiversity of ciliates in the ‘Age of Integration.’. Eur. J. Protistol. 61: 314–322

Cohen J., Adoutte A., Grandchamp S., Houdebine L., Beisson J. (1982) Immunocytochemical study of microtubular structures throughout the cell cycle of Paramecium. Biol. Cell 44: 35e44

Cohen J., Beisson J. (1988) The Cytoskeleton. In: Görtz, H.D. (Ed.), Paramecium. Springer, Berlin, Heidelberg, pp. 363–392

Conner R. L., Koroly M. J. (1973) Chemistry and metabolism of nucleic acids in Tetrahymena. In: Biology of Tetrahymena. Dowden, Hutchinson, and Ross, Inc., Stroudsburg, PA, pp. 123–164

Corliss J. O. (1995) The ambiregnal protists and the codes of nomenclature: a brief review of the problem and of proposed solutions. Bull. zool. nomencl. 52: 11–17

Creevey C. J., Muller J., Doerks T., Thompson J. D., Arendt D., Bork P. (2011) Identifying single copy orthologs in Metazoa. PLoS Comput Biol. 7: e1002269

Dayrat B. (2005) Towards integrative taxonomy. Biol. J. Linn. Soc. 85: 407–415

de Loubresse N. G., Ruiz F., Beisson J., Klotz C. (2001) Role of delta-tubulin and the C-tubule in assembly of Paramecium basal bodies. BMC Cell Biol. 2: 4

Din N., Engberg J. (1979) Extrachromosomal ribosomal RNA genes in Tetrahymena structure and evolution. J. Mol. Biol. 134: 555–574

Dobell C. (1932) Antony van Leeuwenhoek and his “Little animals”, being some account of the father of protozoology and bacteriology and his multifarious discoveries in these disciplines. Harcourt, Brace and company, New York. p. 510

Doerder F. P. (2019) Barcodes reveal 48 new species of Tetrahymena, Dexiostoma, and Glaucoma: phylogeny, ecology, and biogeography of new and established species. J. Eukaryot. Microbiol. 66: 182–208

Dunthorn M., Foissner W., Katz L. A. (2011) Expanding character sampling for ciliate phylogenetic inference using mitochondrial SSU-rDNA as a molecular marker. Protist 162: 85–99

Dunthorn M., Foissner W., Katz L. A. (2008) Molecular phylogenetic analysis of class Colpodea (phylum Ciliophora) using broad taxon sampling. Mol. Phylogenet. Evol. 46: 316–327

Dunthorn M., Hall M., Foissner W., Stoeck T., Katz L. A. (2014a) Broad taxon sampling of ciliates using mitochondrial small subunit ribosomal DNA. Acta Protozool. 53: 207–213

Dunthorn M., Katz L. A. (2008) Richness of morphological hypotheses in ciliate systematics allows for detailed assessment of homology and comparisons with gene trees. Denisia 23: 389–394

Dunthorn M., Katz L. A., Stoeck T., Foissner W. (2012a) Congruence and indifference between two molecular markers for understanding oral evolution in the Marynidae sensu lato (Ciliophora, Colpodea). Eur. J. Protistol. 48: 297–304

Dunthorn M., Klier J., Bunge J., Stoeck T. (2012b) Comparing the hyper-variable V4 and V9 regions of the small subunit rDNA for assessment of ciliate environmental diversity. J. Eukaryot. Microbiol. 59: 185–187

Dunthorn M., Otto J., Berger S. A., Stamatakis A., Mahé F., Romac S., de Vargas C., Audic S., Consortium B., Stock A., Kauff F., Stoeck T. (2014b) Placing environmental next-generation sequencing amplicons from microbial eukaryotes into a phylogenetic context. Mol. Biol. Evol. 31: 993–1009

Dunthorn M., Stoeck T., Clamp J., Warren A., Mahé F. (2014c) Ciliates and the rare biosphere: a review. J. Eukaryot. Microbiol. 61: 404–409

Dupuis-Williams P., Fleury-Aubusson A., de Loubresse N. G., Geoffroy H., Vayssié L., Galvani A., Espigat A., Rossier J. (2002) Functional role of epsilon-tubulin in the assembly of the centriolar microtubule scaffold. J. Cell. Biol. 158: 1183–1193

Eberle J., Ahrens D., Mayer C., Niehuis O., Misof B. (2020) A plea for standardized nuclear markers in metazoan DNA taxonomy. Trends Ecol Evol. 35: 336–345

Eisen J. A., Coyne R. S., Wu M., Wu D., Thiagarajan M., Wortman J. R., Badger J. H., Ren Q., Amedeo P., Jones K. M., Tallon L. J., Delcher A. L., Salzberg S. L., Silva J. C., Haas B. J., Majoros W. H., Farzad M., Carlton J. M., Smith R. K., Garg J., Pearlman R. E., Karrer K. M., Sun L., Manning G., Elde N. C., Turkewitz A. P., Asai D. J., Wilkes D. E., Wang Y., Cai H., Collins K., Stewart B. A., Lee S. R., Wilamowska K., Weinberg Z., Ruzzo W. L., Wloga D., Gaertig J., Frankel J., Tsao C. C., Gorovsky M. A., Keeling P. J., Waller R. F., Patron N. J., Cherry J. M., Stover N. A., Krieger C. J., del Toro C., Ryder H. F., Williamson S. C., Barbeau R. A., Hamilton E. P., Orias E. (2006) Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4: e286

Feng J. M., Jiang C. Q., Warren A., Tian M., Cheng J., Liu G. L., Xiong J., Miao W. (2015) Phylogenomic analyses reveal subclass Scuticociliatia as the sister group of subclass Hymenostomatia within class Oligohymenophorea. Mol. Phylogenet. Evol. 90: 104–111

Fernandes N. M., Campello-Nunes P. H., Paiva T. S., Soraes C. A. G., Silva-Neto I. D. (2021) Ciliate diversity from aquatic environments in the Brazilian Atlantic Forest as revealed by highthroughput DNA sequencing. Microb. Ecol. 81: 630–643

Fernandes N. M., Schrago C.G. (2019) A multigene timescale and diversification dynamics of Ciliophora evolution. Mol. Phylogenet. Evol. 139: 106–521

Fernandez-Galiano D. (1976) Silver impregnation of ciliated protozoa: procedure yielding good results with the pyridinated silver carbonate method. Trans. Am. Microsc. Soc. 95: 557

Foissner W. (2014) An update of ‘basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa’. Int. J. Syst. Evol. Microbiol. 64: 271–292

Foissner W., Agatha S., Berger H. (2002) Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest Africa): with emphasis on two contrasting environments, the Etosha region and the Namib desert. Denisia 5: 1–1063

Forster D., Behnke A., Stoeck T. (2012) Meta-analyses of environmental sequence data identify anoxia and salinity as parameters shaping ciliate communities. Syst. Biodivers. 10: 277–288

Forster D., Bittner L., Karkar S., Dunthorn M., Romac S., Audic S., Lopez P., Stoeck T., Bapteste E. (2015) Testing ecological theories with sequence similarity networks: marine ciliates exhibit similar geographic dispersal patterns as multicellular organisms. BMC Biol. 13: 16

Fu R., Gong J. (2017) Single cell analysis linking ribosomal (r)DNA and rRNA copy numbers to cell size and growth rate provides insights into molecular protistan ecology. J. Eukaryot. Microbiol. 64: 885–896

Gao F., Katz L. A. (2014) Phylogenomic analyses support the bifurcation of ciliates into two major clades that differ in properties of nuclear division. Mol. Phylogenet. Evol. 70: 240–243

Gao F., Li J., Song W., Xu D., Warren A., Yi Z., Gao S. (2016a) Multi-gene-based phylogenetic analysis of oligotrich ciliates with emphasis on two dominant groups: Cyrtostrombidiids and strombidiids (Protozoa, Ciliophora). Mol. Phylogenet. Evol. 105: 241–250

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

Gao Y., Jin S., Dang H., Ye S., Li R. (2018) Mitochondrial genome sequencing of notorious scuticociliates (Pseudocohnilembus persalinus) isolated from Turbot (Scophthalmus maximus L.). Mitochondrial DNA B Resour. 3: 1077–1078

Gentekaki E., Kolisko M., Gong Y., Lynn D. H. (2017) Phylogenomics solves a long-standing evolutionary puzzle in the ciliate world: the subclass Peritrichia is monophyletic. Mol. Phylogenet. Evol. 106: 1–5

Gentekaki E., Lynn D. H. (2009) High-level genetic diversity but no population structure inferred from nuclear and mitochondrial markers of the peritrichous ciliate Carchesium polypinum in the Grand River Basin (North America). Appl. Environ. Microbiol. 75: 3187–3195

Gimmler A., Korn R., de Vargas C., Audic S., Stoeck T. (2016) The Tara Oceans voyage reveals global diversity and distribution patterns of marine planktonic ciliates. Sci. Rep. 6: 33555 Gnirke A., Melnikov A., Maguire J., Rogov P., LeProust E. M., Brockman W., Fennell T., Giannoukos G., Fisher S.,  Russ C., Gabriel S., Jaffe D. B., Lander E. S., Nusbaum C. (2009) Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat Biotechnol. 27: 182–189

Goddard J. M., Cummings D. J. (1975) Structure and replication of mitochondrial DNA from Paramecium aurelia. J. Mol. Biol. 97: 593–609

Gong J., Dong J., Liu X., Massana R. (2013) Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. Protist 164: 369–379.

Gray M. W., Lang B. F., Burger G. (2004) Mitochondria of protists. Annu. Rev. Genet. 38: 477–524

Hauser M., Hausmann K., Jockusch B. M. (1980) Demonstration of tubulin, actin and α-actinin by immunofluorescence in the microtubule-microfilament complex of the cytopharyngeal basket of the ciliate Pseudomicrothorax dubius. Exp. Cell Res. 125: 265–274

Hebert P. D. N., Cywinska A., Ball S. L., deWaard J. R. (2003) Biological identifications through DNA barcodes. Proc. Royal Soc. B. 270: 313–321

Huang Y. X., Wang S., Gao Y. Q., Chen J. H., Wang X. L., Li R. J. (2021) Comparison of mitochondrial genome and development of specific PCR primers for identifying two scuticociliates, Pseudocohnilembus persalinus and Uronema marinum. Parasit. Vectors 14: 318

ICZN (1999) International commission on zoological nomenclature [www document]. URL https://www.iczn.org/the-code/the-international-code-of-zoological-nomenclature/the-code-online/ (accessed 12.10.20) 44 L. Rajter et al.

Iftode F., Cohen J., Ruiz F., Rueda A. T., Chen-Shan L., Adoutte A., Beisson J. (1989) Development of surface pattern during division in Paramecium. I. Mapping of duplication and reorganization of cortical cytoskeletal structures in the wild type. Development 105: 191–211

Iftode F., Fleury A., Adoutte A. (1997) Development of surface pattern during division in Paramecium. Eur. J. Protistol. 33: 145–167

Im K., Mareninov S., Diaz M. F. P., Yong W. H. (2019) An Introduction to Performing Immunofluorescence Staining. In: Yong W. (eds) Biobanking. Methods in Molecular Biology, vol 1897. Humana Press, New York

Jeanmaire-Wolf R., Clérot J.-C., Nahon P., Iftode F., Fleury A., Adoutte A. (1993) Isolation and characterization of monoclonal antibodies to cytoskeletal and membrane proteins of the Paramecium cortex. Eur. J. Protistol. 29: 311–333

Jerka-Dziadosz M., Gogendeau D., Klotz C., Cohen J., Beisson J., Koll F. (2010) Basal body duplication in Paramecium: the key role of Bld10 in assembly and stability of the cartwheel. Cytoskeleton 67: 161–171

Jerka-Dziadosz M., Koll F., Włoga D., Gogendeau D., de Loubresse N. G., Ruiz F., Fabczak S., Beisson J. (2013) A Centrin3-dependent,

transient, appendage of the mother basal body guides the positioning of the daughter basal body in Paramecium. Protist 164: 352–368

Jiang C. Q., Wang G. Y., Xiong J., Yang W. T., Sun Z. Y., Feng J. M., Warren A., Miao W. (2019) Insights into the origin and evolution of Peritrichia (Oligohymenophorea, Ciliophora) based on analyses of morphology and phylogenomics. Mol. Phylogenet. Evol. 132: 25–35

Jung J. H., Moon J. H., Park K. M., Kim S., Dolan J. R., Yang E. J. (2018) Novel insights into the genetic diversity of Parafavella based on mitochondrial CO1 sequences. Zool. Scr. 47: 743–755

Kaczanowska J., Iftode F., Coffe G., Prajer M., Kosciuszko H., Adoutte A. (1996) The protein kinase inhibitor 6-dimethylaminopurine does not inhibit micronuclear mitosis, but impairs the rearrangement of cytoplasmic MTOCs and execution of cytokinesis in the ciliate Paramecium during transition to interphase. Eur. J. Protistol. 32: 2–17

Kahl A. (1931) Urtiere oder Protozoa I: Wimpertiere oder Ciliate (Infusoria) 2. Holotricha (außer den im 1 Teil behandelten Prostomata). In: Dahl, F. (Ed.), Die Tierwelt Deutschlands und der Angrenzenden Meeresteile Nach Ihren Merkmalen und Nach Ihrer Lebensweise, Vol. 2. G. Fischer, Jena, pp. 181–398

Kapli P., Lutteropp S., Zhang J., Kobert K., Pavlidis P., Stamatakis A., Flouri T. (2017) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33: 1630–1638

Kapuscinski J. (1995) DAPI: a DNA-Specific fluorescent probe. Biotech. Histochem. 70: 220–233

Katz L. A., DeBerardinis J., Hall M. S., Kovner A. M., Dunthorn M., Muse S. V. (2011) Heterogeneous rates of molecular evolution among cryptic species of the ciliate morphospecies Chilodonella uncinata. J. Mol. Evol. 73: 266–272

Keryer G., Adoutte A., Ng S. F., Cohen J., de Loubresse N. G., Rossignol M., Stelly N., Beisson J. (1990) Purification of the surface membrane-cytoskeleton complex (cortex) of Paramecium and identification of several of its protein constituents. Eur. J. Protistol. 25: 209–225

Keryer G., Davis F. M., Rao P. N., Beisson J. (1987) Protein phosphorylation and dynamics of cytoskeletal structures associated with basal bodies in Paramecium. Cell Motil. Cytoskel. 8: 44–54

Kirby H. (1945) The structure of the common intestinal trichomonad of man. J. Parasitol. 31: 163–175

Koonin E. V. (2005) Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 39: 309–338

Kovács P., Csaba G. (2006) Comparison of the binding of anti-tubulin antibody and the fluorescent taxol derivative Flutax-1 to the microtubular system of Tetrahymena. Acta Biol. Hung. 57: 323–329

Kress W. J., García-Robledo C., Uriarte M., Erickson D. L. (2015) DNA barcodes for ecology, evolution, and conservation. Trends Ecol. Evol. 30: 25–35

Lai V. C., Ng S. F. (1991) Discrimination of cytoskeletal elements of Paramecium by heterologous antisera: a preliminary investigation on the presence of intermediate filament-related protein. Eur. J. Protistol. 27: 290–305

Lasek-Nesselquist E., Johnson M. D. (2019) A phylogenomic approach to clarifying the relationship of Mesodinium within the Ciliophora: a case study in the complexity of mixed-species transcriptome analyses. Genome Biol. Evol. 11: 3218–3232

Lecke S. B., Tasca T. (2002) Trichomonas vaginalis: microtubule cytoskeleton distribution using fluorescent taxoid. Exp. Parasitol. 102: 113–116

Lessard E. J., Martin M. P., Montagnes D. J. S. (1996) A new method for live-staining protists with DAPI and its application as a tracer of ingestion by walleye pollock (Theragra chalcogramma (Pallas)) larvae. J. Exp. Mar. Biol. Ecol. 204: 43–57

Lewis W. H., Lind A. E., Sendra K. M., Onsbring H., Williams T. A., Esteban G. F., Hirt R. P., Ettema T., Embley T. M. (2020)

Convergent evolution of hydrogenosomes from mitochondria by gene transfer and loss. Mol. Biol. Evol. 37: 524–539

Li R., Gao Y., Hou Y., Ye S., Wang L., Sun J., Li Q. (2018) Mitochondrial genome sequencing and analysis of scuticociliates (Uronema marinum) isolated from Takifugu rubripes. Mitochondrial DNA B Resour. 3: 736–737

Loefer J. B., Scherbaum O. H. (1963) Serological and biochemical factors relative to taxonomy of Tetrahymena. Syst. Biol. 12:  175–177

Luo A., Ling C., Ho S. Y. W., Zhu C. D. (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Syst. Biol. 67: 830–846

Lynn D. H. (2008) The ciliated protozoa: characterization, classification, and guide to the literature. 3rd ed. Springer, Dordrecht Lynn D. H., Doerder F., Gillis P., Prosser R. (2018) Tetrahymena glochidiophila n. sp., a new species of Tetrahymena (Ciliophora) that causes mortality to glochidia larvae of freshwater mussels (Bivalvia). Dis. Aquat. Org. 127: 125–136

Lynn D. H., Kolisko M. (2017) Molecules illuminate morphology: phylogenomics confirms convergent evolution among ‘oligotrichous’ ciliates. Int. J. Syst. Evol. Microbiol. 67: 3676–3682

Lynn D. H., Kolisko M., Bourland W. (2018) Phylogenomic analysis of Nassula variabilis n. sp., Furgasonia blochmanni, and Pseudomicrothorax dubius confirms a nassophorean clade. Protist 169: 180–189

Lynn D. H., Simpson A. G. B. (2009) From the editors: describing new taxa of unicellular protists. J. Eukaryot. Microbiol. 56: 403–405

Lynn D. H., Small E. B. (1981) Protist kinetids: structural conservatism, kinetid structure, and ancestral states. Biosystems 14: 377–385

Lynn D. H., Strüder-Kypke M. C. (2006) Species of Tetrahymena identical by small subunit rRNA gene sequences are discriminated by mitochondrial cytochrome c oxidase I gene sequences. J. Eukaryot. Microbiol. 53: 385–387

Lynn D. H., Suriano D. M., Beverley-Burton M. (1981) Chatton-Lwoff silver impregnation: an improved technique for the study of oncomiracidia (Platyhelminthes: Monogenea) chaetotaxy. Syst. Parasitol. 3: 21–23

McLaughlin N. B., Buhse H. E. (2004) Localization by indirect immunofluorescence of tetrin, actin, and centrin to the oral apparatus and buccal cavity of the macrostomal form of Tetrahymena vorax. J. Eukaryot. Microbiol. 51: 253–257

McManus G. B., Katz L. A. (2009) Molecular and morphological methods for identifying plankton: what makes a successful marriage? J. Plankton Res. 31: 1119–1129

Medina X. S., Macek M., Bautista-Reyes F., Perz A., Lemus P. B., Arteaga M. C. (2016) Inter-annual ciliate distribution variation within the late stratification oxycline in a monomictic lake, Lake Alchichica (Mexico). J. Limnol. 75: 179–190

Mohr M., Ruthmann A., Eichenlaub-Ritter U., Kühn S., Traub P. (1990) Evidence for intermediate-like filaments in a heterotrichous ciliate. Eur. J. Protistol. 25: 255–263

Montagnes D. J. S., Lynn D. H. (1987) A Quantitative Protargol Stain (QPS) for ciliates: method description and test of its quantitative nature. Mar. Microb. Food Webs 2: 83–93

Morard R., Escarguel G., Weiner A. K. M., André A., Douady C. J., Wade C. M., Darling K. F., Ujiié Y., Seears H. A., Quillévéré F., de Garidel-Thoron T., de Vargas C., Kucera M. (2016) Nomenclature for the nameless: a proposal for an integrative molecular taxonomy of cryptic diversity exemplified by planktonic Foraminifera. Syst. Biol. 65: 925–940

Morin G. B., Cech T. R. (1988) Mitochondrial telomeres: surprising diversity of repeated telomeric DNA sequences among six species of Tetrahymena. Cell 52: 367–374

Mullis K. B., Faloona F. A. (1987) Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 155: 335–350

Nanney D. L. (1977) Molecules and morphologies: the perpetuation of pattern in the ciliated protozoa. J. Protozool. 24: 27–35

Nanney D. L., Meyer E. B., Simon E. M., Preparata R. M. (1989) Comparison of ribosomal and isozymic phylogenies of tetrahymenine ciliates. J. Protozool. 36: 1–8

Nelson D. L. (1995) Preparation of cilia and subciliary fractions from Paramecium. Methods Cell Biol. 47: 17–24

Obert T., Vďačný P. (2020) Delimitation of five astome ciliate species isolated from the digestive tube of three ecologically different groups of lumbricid earthworms, using the internal transcribed spacer region and the hypervariable D1/D2 region of the 28S rRNA gene. BMC Evol. Biol. 20: 37

Pan X., Bourland W. A., Song W. (2013) Protargol synthesis: an inhouse protocol. J. Eukaryot. Microbiol. 60: 609–614

Park M. H., Jung J. H., Jo E., Park K. M., Baek Y. S., Kim S. J., Min G. S. (2019) Utility of mitochondrial CO1 sequences for species discrimination of Spirotrichea ciliates (Protozoa, Ciliophora). Mitochondrial DNA, Part A 30: 148–155

Pfister G., Sonntag B., Posch T. (1999) Comparison of a direct live count and an improved quantitative protargol stain (QPS) in determining abundance and cell volumes of pelagic freshwater protozoa. Aquat. Microb. Ecol. 18: 95–103

Pitsch G., Bruni E. P., Forster D., Qu Z., Sonntag B., Stoeck T., Posch T. (2019) Seasonality of planktonic freshwater ciliates: are analyses based on V9 regions of the 18S rRNA gene correlated with morphospecies counts? Front. Microbiol. 10: 248

Preparata R. M., Meyer E. B., Preparata F. P., Simon E. M., Vossbrinck C. R., Nanney D. L. (1989) Ciliate evolution: The ribosomal phylogenies of the tetrahymenine ciliates. J. Mol. Evol. 28: 427–441

Pruitt K. D., Tatusova T., Maglott D. R. (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35: D61–D65

Rotterová J., Salomaki E., Pánek T., Bourland W., Žihala D., Táborský P., Edgcomb V. P., Beinart R. A., Kolísko M., Čepička I. (2020) Genomics of new ciliate lineages provides insight into the evolution of obligate anaerobiosis. Curr. Biol. 30: 2037-2050.e6

Ruiz F., Beisson J., Rossier J., Dupuis-Williams P. (1999) Basal body duplication in Paramecium requires gamma-tubulin. Curr. Biol. 9: 43–46

Ruiz F., Dupuis-Williams P., Klotz C., Forquignon F., Bergdoll M., Beisson J., Koll F. (2004) Genetic evidence for interaction between η- and β-tubulins. Eukaryot. Cell 3: 212–220

Ruiz F., de Loubresse N. G., Klotz C., Beisson J., Koll F. (2005) Centrin deficiency in Paramecium affects the geometry of basal-body duplication. Curr. Biol. 15: 2097–2106

Sadler L. A., Brunk C. F. (1992) Phylogenetic relationships and unusual diversity in histone H4 proteins within the Tetrahymena pyriformis complex. Mol. Phylogenet. Evol. 9: 70–84

Sanger F., Nicklen S., Coulson A. R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 74: 5463–5467

Santoferrara L. F., Bachy C., Alder V. A., Gong J., Kim Y.-O., Saccà A., Neto I. D. da S., Strüder‐Kypke M. C., Warren A., Xu D., Yi Z., Agatha S. (2016) Updating biodiversity studies in loricate protists: the case of the tintinnids (Alveolata, Ciliophora, Spirotrichea). J. Eukaryot. Microbiol. 63: 651–656

Santoferrara L. F., Burki F., Filker S., Logares R., Dunthorn M., McManus G. B. (2020) Perspectives from ten years of protist studies by high-throughput metabarcoding. J. Eukaryot. Microbiol. 67: 612–622

Santoferrara L. F., Tian M., Alder V. A., McManus G. B. (2015) Discrimination of closely related species in tintinnid ciliates: new insights on crypticity and polymorphism in the genus Helicostomella. Protist 166: 78–92

Shazib S. U. A., Vďačný P., Kim J. H., Jang S. W., Shin M. K. (2016) Molecular phylogeny and species delimitation within the ciliate genus Spirostomum (Ciliophora, Postciliodesmatophora, Heterotrichea), using the internal transcribed spacer region. Mol. Phylogenet. Evol. 102: 128–144

Skibbe O. (1994) An improved quantitative protargol stain for ciliates and other planktonic protists. Arch. Hydrobiol. 130: 339–347

Smith D. R. (2016) The past, present and future of mitochondrial genomics: have we sequenced enough mtDNAs? Brief. Funct. Genomics 15: 47–54

Smith D. R., Keeling P. J. (2015) Mitochondrial and plastid genome architecture: reoccurring themes, but significant differences at the extremes. Proc. Natl. Acad. Sci. U. S. A. 112: 10177–10184

Sogin M. L., Ingold A., Karlok M., Nielsen H., Engberg J. (1986) Phylogenetic evidence for the acquisition of ribosomal RNA introns subsequent to the divergence of some of the major  Tetrahymena groups. EMBO J. 5: 3625–3630

Sperling L., Keryer G., Ruiz F., Beisson J. (1991) Cortical morphogenesis in Paramecium: A transcellular wave of protein phosphorylation involved in ciliary rootlet disassembly. Dev. Biol. 148: 205–218

Stockert J. C., Blazquez-Castro A. (2017) Dyes and fluorochromes. In: Stockert J. C. & Blazquez-Castro A., Fluorescence Microscopy in Life Sciences., Bentham Science Publishers, pp. 61–95

Stoeck T. (2018) Metabarcoding of benthic ciliate communities shows high potential for environmental monitoring in salmon aquaculture. Ecol. Indic. 85: 153–164

Stoeck T., Przybos E., Dunthorn M. (2014) The D1-D2 region of the large subunit ribosomal DNA as barcode for ciliates. Mol. Ecol. Resour. 14: 458–468

Strüder-Kypke M. C., Lynn D. H. (2010b) 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. System. Biodivers. 8: 131–148

Sun Z., Jiang C., Feng J., Yang W., Li M., Miao W. (2017) Phylogenomic analysis of Balantidium ctenopharyngodoni (Ciliophora, Litostomatea) based on single-cell transcriptome sequencing. Parasite 24: 43

Suyama Y., Miura K. (1968) Size and structural variations of mitochondrial DNA. Proc. Natl. Acad. Sci. U. S. A. 60: 235–242

Swart E. C., Nowacki M., Shum J., Stiles H., Higgins B. P., Doak T. G., Schotanus K., Magrini V. J., Minx P., Mardis E. R., Landweber L. F. (2012) The Oxytricha trifallax mitochondrial genome. Genome Biol. Evol. 4: 136–154

Taberlet P., Bonin A., Zinger L., Coissac E. (2018) Environmental DNA: for biodiversity research and monitoring, environmental DNA. Oxford University Press. p. 1–272

Tice A. K., Žihala D., Pánek T., Jones R. E., Salomaki E. D., Nenarokov S., Burki F., Eliáš M., Eme L., Roger A. J., Rokas A., Shen X. X., Strassert J., Kolísko M., Brown M. W. (2021) PhyloFisher: a phylogenomic package for resolving eukaryotic relationships. PLoS biol. 19: e3001365

Van Wichelen J., Johansson L. S., Vanormelingen P., Declerck S. A. J., Lauridsen T. L., De Meester L., Jeppesen E., Vyverman W. (2013) Planktonic ciliate community structure in shallow lakes of lowland Western Europe. Eur. J. Protistol. 49: 538–551

Vďačný P. (2017) Integrative taxonomy of ciliates: assessment of molecular phylogenetic content and morphological homology testing. Eur. J. Protistol. 61: 388–398

Vďačný P., Foissner W. (2019) Re-analysis of the 18S rRNA gene phylogeny of the ciliate class Colpodea. Eur. J. Protistol. 67: 89–105

Venter P. C., Nitsche F., Scherwass A., Arndt H. (2018) Discrepancies between molecular and morphological databases of soil ciliates studied for temperate grasslands of Central Europe. Protist 169: 521–538

Wancura M. M., Yan Y., Katz L. A., Maurer-Alcalá X. X. (2018) Nuclear features of the heterotrich ciliate Blepharisma americanum: genomic amplification, life cycle, and nuclear inclusion. J. Eukaryot. Microbiol. 65: 4–11

Wang C., Hu Y., Warren A., Hu X. (2021) Genetic diversity and phylogeny of the genus Euplotes (Protozoa, Ciliophora) revealed by the mitochondrial CO1 and nuclear ribosomal genes. Microorganisms 9: 2204

Wang P., Wang Y., Wang C., Zhang T., Al-Farraj S. A., Gao F. (2017) Further consideration on the phylogeny of the Ciliophora: Analyses using both mitochondrial and nuclear data with focus on the extremely confused class Phyllopharyngea. Mol. Phylogenet. Evol. 112: 96–106

Wang Y., Jiang Y., Liu Y., Li Y., Katz L. A., Gao F., Yan Y. (2020) Comparative studies on the polymorphism and copy number variation of mtSSU rDNA in ciliates (Protista, Ciliophora): implications for phylogenetic, environmental, and ecological research. Microorganisms 8: 316

Wang Y., Wang C., Jiang Y., Katz L. A., Gao F., Yan Y. (2019) Further analyses of variation of ribosome DNA copy number and polymorphism in ciliates provide insights relevant to studies of both molecular ecology and phylogeny. Sci China Life Sci. 62: 203–214

Warren A., Patterson D. J., Dunthorn M., Clamp J. C., Achilles-Day U. E. M., Aescht E., Al-Farraj S. A., Al-Quraishy S., Al-Rasheid K., Carr M., Day J. G., Dellinger M., El-Serehy H. A., Fan Y., Gao F., Gao S., Gong J., Gupta R., Hu X., Kamra K., Langlois G., Lin X., Lipscomb D., Lobban C. S., Luporini P., Lynn D. H., Ma H., Macek M., Mackenzie-Dodds J., Makhija S., Mansergh R. I., Martín-Cereceda M., McMiller N., Montagnes D. J. S., Nikolaeva S., Ong’ondo G. O., Pérez-Uz B., Purushothaman J., Quintela-Alonso P., Rotterová J., Santoferrara L., Shao C., Shen Z., Shi X., Song W., Stoeck T., La Terza A., Vallesi A., Wang M., Weisse T., Wiackowski K., Wu L., Xu K., Yi Z., Zufall R., Agatha S. (2017) Beyond the “code”: a guide to the description and documentation of biodiversity in ciliated protists (Alveolata, Ciliophora). J. Eukaryot. Microbiol. 64: 539–554

Wickham S., Gieseke A., Berninger U. (2000) Benthic ciliate identification and enumeration: an improved methodology and its application. Aquat. Microb. Ecol. 22: 79–91

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

Xu D., Sun P., Shin M. K., Kim Y. O. (2012) Species boundaries in tintinnid ciliates: a case study –morphometric variability, molecular characterization, and temporal distribution of Helicostomella species (Ciliophora, Tintinnina). J. Eukaryot. Microbiol. 59: 351–358

Yang J., Huang S., Fan W., Warren A., Jiao N., Xu D. (2020) Spatial distribution patterns of planktonic ciliate communities in the East China Sea: Potential indicators of water masses. Mar. Pollut. Bull. 156: 111253

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

Zhao F., Filker S., Xu K., Li J., Zhou T., Huang P. (2019) Effects of intragenomic polymorphism in the SSU rRNA gene on estimating marine microeukaryotic diversity: A test for ciliates using single‐cell high‐throughput DNA sequencing. Limnol. Oceanogr.: Methods 17: 533–543

Zhao F., Xu K. (2016) Biodiversity patterns of soil ciliates along salinity gradients. Eur. J. Protistol. 53: 1–10

Zhao Y., Gentekaki E., Yi Z., Lin X. (2013) Genetic differentiation of the mitochondrial cytochrome oxidase c subunit I gene in genus Paramecium (Protista, Ciliophora). PLoS One 8: e77044

Zhao Y., Yi Z., Gentekaki E., Zhan A., Al-Farraj S. A., Song W. (2016) Utility of combining morphological characters, nuclear and mitochondrial genes: an attempt to resolve the conflicts of species identification for ciliated protists. Mol. Phylogenet. Evol. 94: 718–729

Information

Information: Acta Protozoologica, 2022, pp. 35 - 46

Article type: Original research article

Authors

Phycology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany

Eukaryotic Microbiology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany

Institute of Evolution and Marine Biodiversity & College of Fisheries, Ocean University of China, Qingdao, China

Eukaryotic Microbiology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany

Natural History Museum, University of Oslo, Oslo, Norway

Eukaryotic Microbiology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany

Published at: 2022

Article status: Open

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Percentage share of authors:

Ľubomír Rajter (Author) - 25%
Borong Lu (Author) - 25%
Erika Rassoshanska (Author) - 25%
Micah Dunthorn (Author) - 25%

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