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Multi-gene phylogeny of Tetrahymena refreshed with three new histophagous species invading freshwater planarians

  • Genetics, Evolution, and Phylogeny - Original Paper
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Abstract

Planarians represent an insufficiently explored group of aquatic invertebrates that might serve as hosts of histophagous ciliates belonging to the hymenostome genus Tetrahymena. During our extensive research on freshwater planarians, parasitic tetrahymenas were detected in two of the eight planarian species investigated, namely, in Dugesia gonocephala and Girardia tigrina. Using the 16S and 18S rRNA genes as well as the barcoding cytochrome oxidase subunit I, one ciliate species was identified as T. scolopax and three species were recognized as new forms: T. acanthophora, T. dugesiae, and T. nigricans. Thus, 25% of the examined planarian taxa are positive for Tetrahymena species and three of them represent new taxa, indicating a large undescribed ciliate diversity in freshwater planarians. According to phylogenetic analyses, histophagous tetrahymenas show a low phylogenetic host specificity. Although T. acanthophora, T. dugesiae, and T. scolopax clustered together within the “borealis” clade, the former species has been detected exclusively in G. tigrina, while the two latter species only in D. gonocephala. Tetrahymena nigricans, which has been isolated only from G. tigrina, was classified within the “paravorax” clade along with T. glochidiophila which feeds on glochidia. The present phylogenetic reconstruction of ancestral life strategies suggested that the last common ancestor of the family Tetrahymenidae was free-living, unlike the progenitor of the subclass Hymenostomatia which was very likely parasitic. Consequently, there were at least seven independent shifts back to parasitism/histophagy within Tetrahymena: one each in the “paravorax” and “australis” clades and at least five transfers back to parasitism in the “borealis” clade.

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Acknowledgments

We thank two anonymous reviewers for their valuable comments. We are also grateful to Ján Kočišek, Erik Mravec, Ivan Rúrik, Martin Sečanský, Eva Tirjaková, and Michal Veselický for their help with sampling, and to Ivan Rúrik for his help with some bioinformatics tools.

Funding

This work was supported by the Slovak Research and Development Agency under the contract no. APVV-15-0147, by the Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic and Slovak Academy of Sciences under the Grant VEGA 1/0041/17, and by the Comenius University in Bratislava under the Grant UK/160/2020.

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Correspondence to Matej Rataj.

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All applicable institutional, national, and international guidelines for the care and use of animals were followed.

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The authors declare that they have no conflict of interest.

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Rataj, M., Vďačný, P. Multi-gene phylogeny of Tetrahymena refreshed with three new histophagous species invading freshwater planarians. Parasitol Res 119, 1523–1545 (2020). https://doi.org/10.1007/s00436-020-06628-0

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  • DOI: https://doi.org/10.1007/s00436-020-06628-0

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