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Ultrastructural Studies on a Model Tintinnid - Schmidingerella meunieri (Kofoid and Campbell, 1929) Agatha and Strüder-Kypke, 2012 (Ciliophora). I. Somatic Kinetids with Unique Ultrastructure

Publication date: 11.01.2019

Acta Protozoologica, 2018, Volume 57, Issue 3, pp. 195 - 214

https://doi.org/10.4467/16890027AP.18.015.10091

Authors

,
Michael S. Gruber
Department of Biosciences, University of Salzburg, Salzburg, Austria
All publications →
,
Alexandra Mühlthaler
Department of Biosciences, University of Salzburg, Salzburg, Austria
All publications →
Sabine Agatha
Department of Biosciences, University of Salzburg, Salzburg, Austria
Department of Organismic Biology, University of Salzburg, Salzburg, Austria
All publications →

Titles

Ultrastructural Studies on a Model Tintinnid - Schmidingerella meunieri (Kofoid and Campbell, 1929) Agatha and Strüder-Kypke, 2012 (Ciliophora). I. Somatic Kinetids with Unique Ultrastructure

Abstract

Molecular phylogenies of Oligotrichea currently do not contain all genera and families and display topologies which are often incongruent with morphological findings. In ciliates, the somatic kinetids are rather conserved, i.e., their ultrastructures, particularly the fibrillar associates, often characterise the main groups, except for the choreotrichids. Four  different kinetid types are found in protargolstained choreotrichids and used for reconstructing the taxon’s evolution (the “Kinetid Transformation Hypothesis”). Proof for this hypothesis requires transmission electron microscopic studies, which are very rare in the choreotrichids and oligotrichids. Such an approach provides insights into the ultrastructural variability of somatic kinetids in spirotrichs and may also detect apomorphies characterising certain choreotrichid families. In the model tintinnid Schmidingerella meunieri, the ultrastructure of the three kinetid types in the somatic ciliature is studied in cryofixed cells. The data support the “Kinetid Transformation Hypothesis” regarding  tintinnids with a ventral kinety. This first detailed study on kinetids in tintinnids and choreotrichids in general reveals totally new kinetid types in ciliates: beyond the three common associates, they are characterised by two or three conspicuous microtubular ribbons extending on the kinetids’ left sides. These extraordinary ribbons form together with the overlapping postciliary ribbons a unique network in the cortex of the anterior cell portion. The evolutionary constrains which might have fostered the development of such structures are discussed for the Oligotrichea, the choreotrichids, and tintinnids as their first occurrence is currently uncertain. Additionally, the kinetids in tintinnids, aloricate  choreotrichids, oligotrichids, hypotrichs, and euplotids are compared.

References

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Agatha S. (2004) Evolution of ciliary patterns in the Oligotrichida (Ciliophora, Spirotricha) and its taxonomic implications. Zoology 107: 153–168

Agatha S. (2011) Updated hypothesis on the evolution of oligo­trichid ciliates (Ciliophora, Spirotricha, Oligotrichida) based on somatic ciliary patterns and ontogenetic data. Eur. J. Protistol. 47: 51–56

Agatha S., Strüder-Kypke M. C. (2007) Phylogeny of the order Choreotrichida (Ciliophora, Spirotricha, Oligotrichea) as inferred from morphology, ultrastructure, ontogenesis, and SSrRNA gene sequences. Eur. J. Protistol. 43: 37–63

Agatha S., Strüder-Kypke M. C. (2012) Reconciling cladistic and genetic analyses in choreotrichid ciliates (Ciliophora, Spirotricha, Oligotrichea). J. Eukaryot. Microbiol. 59: 325–350

Agatha S., Strüder-Kypke M. C. (2014) What morphology and molecules tell us about the evolution of Oligotrichea (Alveolata, Ciliophora). Acta Protozool. 53: 77–90

Chaaban S., Brouhard G. J. (2017) A microtubule bestiary: structural diversity in tubulin polymers. Mol. Biol. Cell 28: 2924–2931

Dave D., Wloga D., Sharma N., Gaertig J. (2009) DYF-1 Is required for assembly of the axoneme in Tetrahymena thermophilaEukaryot. Cell 8: 1397–1406

Deitmer J. W., Machemer H., Martinac B. (1984) Motor control in three types of ciliary organelles in the ciliate StylonychiaJ. Comp. Physiol. A 154: 113–120

Echevarria M. L., Wolfe G. V., Strom S. L., Taylor A. R. (2014) Connecting alveolate cell biology with trophic ecology in the marine plankton using the ciliate Favella as a model. FEMS Microbiol. Ecol. 90: 18–38

Echevarria M. L., Wolfe G. V., Taylor A. R. (2016) Feast or flee: bio­electrical regulation of feeding and predator evasion behaviors in the planktonic alveolate Favella sp. (Spirotrichia). J. Exp. Biol. 219: 445–456

Ehrenberg C. G. (1830) Organisation, Systematik und geographi­sches Verhältnis der Infusionsthierchen. Zwei Vorträge, in der Akademie der Wissenschaften zu Berlin gehalten in den Jahren 1828 und 1830. Druckerei der Königlichen Akademie der Wissenschaften, Berlin: 1–108 + Plate I–VIII

Eisler K. (1988) Electron microscopical observations on the ciliate Furgasonia blochmanni Fauré-Fremiet, 1967. Part I: An update on morphology. Eur. J. Protistol. 24: 75–93

Eisler K. (1989) Electron microscopical observations on the ciliate Furgasonia blochmanni Fauré-Fremiet, 1967. Part II: Morphogenesis and phylogenetic conclusions. Eur. J. Protistol. 24: 181–199

Fauré-Fremiet E. (1924) Contribution à la connaissance des infusoires planktoniques. Bull. biol. Fr. Belg. Suppl. 6: 1–171

Fauré-Fremiet E., Ganier M.-C. (1970) Structure fine du Strombidium sulcatum Cl. et L. (Ciliata Oligotrichida). Protistologica 6: 207–223

Fleury A., Iftode F., Deroux G., Fryd-Versavel G. (1985) Unité et diversité chez les hypotriches (Protozoaires Ciliés): II – Éléments d’ultrastructure comparée chez divers represéntants du sous-ordre des Euhypotrichina. Protistologica 21: 505–524

Foissner W., Moon-van der Staay S. Y., van der Staay G. W. M., Hackstein J. H. P., Krautgartner W.-D., Berger H. (2004) Reconciling classical and molecular phylogenies in the stichotrichines (Ciliophora, Spirotrichea), including new sequences from some rare species. Eur. J. Protistol. 40: 265–281

Gentekaki E., Kolisko M., Boscaro V., Bright K. J., Dini F., Di Giuseppe G., Gong Y., Miceli C., Modeo L., Molestina R. E., Petroni G., Pucciarelli S., Roger A. J., Strom S. L., Lynn D. H. (2014) Large-scale phylogenomic analysis reveals the phylogenetic position of the problematic taxon Protocruzia and unravels the deep phylogenetic affinities of the ciliate lineages. Mol. Phylogenet. Evol. 78: 36–42

Gerassimova Z., Seravin L. (1976) Ectoplasmic fibrillar system of Infusoria and its role for the understanding of their phylogeny. Zool. Zh. 55: 645–656

Görtz H.-D. (1982) The behavior and fine structure of the dorsal bristles of Euplotes minuta, E. aediculatus, and Stylonychia mytilus (Ciliata, Hypotrichida). J. Protozool. 29: 353–359

Grim J. N. (1987) The kinetid structures of the choreotrichous ciliate Strobilidium velox and an assessment of its evolutionary lineage. J. Protozool. 34: 117–123

Grimes G. W., Adler J. A. (1976) The structure and development of the dorsal bristle complex of Oxytricha fallax and Stylonychia pustulataJ. Protozool. 23: 135–143

Gruber M. S., Strüder-Kypke M., Agatha S. (2018) Redescription of Tintinnopsis everta Kofoid and Campbell 1929 (Alveolata, Ciliophora, Tintinnina) based on taxonomic and genetic analyses – discovery of a new complex ciliary pattern. J. Eukaryot. Microbiol. 65: 484–504

Guillard R. R. L. (1975) Culture of phytoplankton for feeding marine invertebrates. In: Culture of Marine Invertebrate Animals, (Eds. W. L. Smith, M. H. Chanley). Plenum Press, New York, London, 29–60

Hedin H. (1976) Microtubules and microfilaments in the tintinnid ciliate Ptychocylis minor Jörgensen. Zoon 4: 3–10

Kilburn C., Winey M. (2008) Basal bodies. Curr. Biol. 18: R56–R57

Kim S. Y., Yang E. J., Gong J., Choi J. K. (2010) Redescription of Favella ehrenbergii (Claparède and Lachmann, 1858) Jörgen­sen, 1924 (Ciliophora: Choreotrichia), with phylogenetic analyses based on small subunit rRNA gene sequences. J. Eukaryot. Microbiol. 57: 460–467

Kofoid C. A., Campbell A. S. (1929) A conspectus of the marine and fresh-water Ciliata belonging to the suborder Tintinnoinea, with descriptions of new species principally from the Agassiz Expedition to the eastern tropical Pacific 1904–1905. Univ. Calif. Publs Zool. 34: 1–403

Laval-Peuto M., Brownlee D. C. (1986) Identification and systematics of the Tintinnina (Ciliophora): evaluation and suggestions for improvement. Ann. Inst. océanogr., Paris 62: 69–84

Lenzi P., Rosati G. (1993) Ultrastructural study of Euplotidium itoi (Ciliata Hypotrichida). Eur. J. Protistol. 29: 453–461

Lynn D. H. (1981) The organization and evolution of microtubular organelles in ciliated protozoa. Biol. Rev. 56: 243–292

Lynn D. H. (1996) My journey in ciliate systematics. J. Eukaryot. Microbiol. 43: 253–260

Lynn D. H. (2008) The Ciliated Protozoa. Characterization, Classification, and Guide to the Literature. Springer

Lynn D. H. (2017) Ciliophora. In: Handbook of the Protists, (Eds. J. M. Archibald, A. G. B. Simpson, C. H. Slamovits)2nd ed. Springer International Publishing: 1, 679–730

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

Meunier A. (1919) Microplankton de la mer Flamande: les Tintinnides et caetera. Mém. Mus. r. Hist. nat. Belg. 8: 1–59 + Plates XXII, XXIII

Modeo L., Petroni G., Bonaldi M., Rosati G. (2001) Trichites of Strombidium (Ciliophora, Oligotrichida) are extrusomes. J. Eukaryot. Microbiol. 48: 95–101

Modeo L., Petroni G., Rosati G., Montagnes D. J. S. (2003) A multidisciplinary approach to describe protists: redescriptions of Novistrombidium testaceum Anigstein 1914 and Strombidium inclinatum Montagnes, Taylor, and Lynn 1990 (Ciliophora, Oligotrichia). J. Eukaryot. Microbiol. 50: 175–189

Modeo L., Petroni G., Lobban C. S., Verni F., Vannini C. (2013) Morphological, ultrastructural, and molecular characterization of Euplotidium rosati n. sp (Ciliophora, Euplotida) from Guam. J. Eukaryot. Microbiol. 60: 25–36

Montagnes D. J. S. (1996) Growth responses of planktonic ciliates in the genera Strobilidium and StrombidiumMar. Ecol. Prog. Ser. 130: 241–254

Morelli A., Giambelluca A., Lenzi P., Rosati G., Verni F. (1996) Ultrastructural features of the peculiar filter-feeding hypotrich ciliate Uronychia transfugaMicron 27: 399–406

Petz W., Foissner W. (1992) Morphology and morphogenesis of Strobilidium caudatum (Fromentel), Meseres corlissi n. sp., Halteria grandinella (Müller), and Strombidium rehwaldi n. sp., and a proposed phylogenetic system for oligotrich ciliates (Protozoa, Ciliophora). J. Protozool. 39: 159–176

Petz W., Song W., Wilbert N. (1995) Taxonomy and ecology of the ciliate fauna (Protozoa, Ciliophora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Stapfia 40: 1–223

Raikov I. B., Gerassimova-Matvejeva Z. P., Puytorac P. de (1975) Cytoplasmic fine structure of the marine psammobiotic ciliate Tracheloraphis dogieli Raikov. I. Somatic infraciliature and cortical organelles. Acta Protozool. 14: 17–42

Rajter L., Vďačný P. (2018) Selection and paucity of phylogenetic signal challenge the utility of alpha-tubulin in reconstruction of evolutionary history of free-living litostomateans (Protista, Ciliophora). Mol. Phylogenet. Evol. 127: 534–544

Ruffolo J. J., Jr. (1976) Fine structure of the dorsal bristle complex and pellicle of EuplotesJ. Morph. 148: 469–487

Santoferrara L. F., Alder V. V., McManus G. B. (2017) Phylogeny, classification and diversity of Choreotrichia and Oligotrichia (Ciliophora, Spirotrichea). Mol. Phylogenet. Evol. 112: 12–22

Small E. B., Lynn D. H. (1985) Phylum Ciliophora Doflein, 1901. In: An Illustrated Guide to the Protozoa, (Eds. J. J. Lee, S. H. Hutner, E. C. Bovee). Society of Protozoologists, Allen Press, Lawrence, Kansas, 393–575

Strom S. L., Wolfe G. V., Bright K. J. (2007) Responses of marine planktonic protists to amino acids: feeding inhibition and swimming behavior in the ciliate Favella sp. Aquat. Microb. Ecol. 47: 107–121

Wicklow B. J. (1983) Ultrastructure and cortical morphogenesis in the euplotine hypotrich Certesia quadrinucleata Fabre-Domergue, 1885 (Ciliophora, Protozoa). J. Protozool. 30: 256–266

Information

Information: Acta Protozoologica, 2018, Volume 57, Issue 3, pp. 195 - 214

Article type: Original article

Authors

Department of Biosciences, University of Salzburg, Salzburg, Austria

Department of Biosciences, University of Salzburg, Salzburg, Austria

Department of Biosciences, University of Salzburg, Salzburg, Austria

Department of Organismic Biology, University of Salzburg, Salzburg, Austria

Published at: 11.01.2019

Article status: Open

Licence: CC BY-NC-ND  licence icon

Percentage share of authors:

Michael S. Gruber (Author) - 33%
Alexandra Mühlthaler (Author) - 33%
Sabine Agatha (Author) - 34%

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