New Parabasalia symbionts Snyderella spp. and Daimonympha gen. nov. from South American Rugitermes termites and the parallel evolution of a cell with a rotating "head"

. 2023 Sep-Oct ; 70 (5) : e12987. [epub] 20230619

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37282792

Most Parabasalia are symbionts in the hindgut of "lower" (non-Termitidae) termites, where they widely vary in morphology and degree of morphological complexity. Large and complex cells in the class Cristamonadea evolved by replicating a fundamental unit, the karyomastigont, in various ways. We describe here four new species of Calonymphidae (Cristamonadea) from Rugitermes hosts, assigned to the genus Snyderella based on diagnostic features (including the karyomastigont pattern) and molecular phylogeny. We also report a new genus of Calonymphidae, Daimonympha, from Rugitermes laticollis. Daimonympha's morphology does not match that of any known Parabasalia, and its SSU rRNA gene sequence corroborates this distinction. Daimonympha does however share a puzzling feature with a few previously described, but distantly related, Cristamonadea: a rapid, smooth, and continuous rotation of the anterior end of the cell, including the many karyomastigont nuclei. The function of this rotatory movement, the cellular mechanisms enabling it, and the way the cell deals with the consequent cell membrane shear, are all unknown. "Rotating wheel" structures are famously rare in biology, with prokaryotic flagella being the main exception; these mysterious spinning cells found only among Parabasalia are another, far less understood, example.

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Boscaro, V., James, E.R., Fiorito, R., Hehenberger, E., Karnkowska, A., del Campo, J. et al. (2017) Molecular characterization and phylogeny of four new species of the genus Trichonympha (Parabasalia, Trichonymphea) from lower termite hindguts. International Journal of Systematic and Evolutionary Microbiology, 67, 3570-3575. Available from: https://doi.org/10.1099/ijsem.0.002169

Brugerolle, G. (1986) Structural diversity of trichomonads as the basis for systematic and evolutionary considerations. Acta Universitatis Carolinae Biologica, 30, 199-210. Available from: https://doi.org/10.1016/j.ijpara.2007.07.018

Brugerolle, G. & Lee, J.J. (2000) Phylum Parabasalia. In: Lee, J.J., Leedale, G.F. & Bradbury, P.C. (Eds.) An illustrated guide to the protozoa: organisms traditionally referred to as protozoa, or newly discovered groups. Lawrence, KS: Society of Protozoologists, pp. 1196-1250.

Brugerolle, G. & Patterson, D.J. (2001) Ultrastructure of Joenina pulchella Grassi, 1917 (Protista, Parabasalia), a reassessment of evolutionary trends in the parabasalids, and a new order Cristamonadida for devescovinid, calonymphid and lophomonad flagellates. Organisms, Diversity and Evolution, 1, 147-160. Available from: https://doi.org/10.1078/1439-6092-00012

Cepicka, I., Hampl, V. & Kulda, J. (2010) Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist, 161, 400-433. Available from: https://doi.org/10.1016/j.protis.2009.11.005

Céza, V., Kotyk, M., Kubánková, A., Yubuki, N., Štáhlavsky, F., Silberman, J.D. et al. (2022) Free-living trichomonads are unexpectedly diverse. Protist, 173, 125883. Available from: https://doi.org/10.1016/j.protis.2022.125883

d'Ambrosio, U., Dolan, M., Wier, A.M. & Margulis, L. (1999) Devescovinid trichomonad with axostyle-based rotary motor (‘rubberneckia’): taxonomic assignment as Caduceia versatilis sp. nov. European Journal of Protistology, 35, 327-337. Available from: https://doi.org/10.1016/S0932-4739(99)80011-X

de Mello, I.F. (1954) Contribution à l'étude des microparasites de termites brésiliens. II. Un nouveau Calonymphide, “Snyderella ypiranga” sp. n., de “Rugitermes rugosus” (Hagen 1858). Revista Brasileira de Biologia, 14, 71-78.

del Campo, J., James, E.R., Hirakawa, Y., Fiorito, R., Kolisko, M., Irwin, N.A.T. et al. (2017) Pseudotrichonympha leei, Pseudotrichonympha lifesoni, and Pseudotrichonympha pearti, new species of parabasalian flagellates and the description of a rotating subcellular structure. Scientific Reports, 7, 16349. Available from: https://doi.org/10.1038/s41598-017-16259-8

Dolan, M.F., d'Ambrosio, U., Wier, A.M. & Margulis, L. (2000) Surface kinetosomes and disconnected nuclei of a calonymphid: ultrastructure and evolutionary significance of Snyderella tabogae. Acta Protozoologica, 39, 135-141.

Foà, A. (1905) Due nuovi flagellati parassiti. Atti della Reale Accademia dei Lincei, 14, 542-546.

Gile, G.H., James, E.R., Okamoto, N., Carpenter, K.J., Scheffrah, R.H. & Keeling, P.J. (2015) Molecular evidence for the polyphyly of Macrotrichomonas (Parabasalia: Cristamonadea) and a proposal for Macrotrichomonoides n. gen. The Journal of Eukaryotic Microbiology, 62, 494-504. Available from: https://doi.org/10.1111/jeu.12204

Gile, G.H., James, E.R., Scheffrahn, R.H., Carpenter, K.J., Harper, J.T. & Keeling, P.J. (2011) Molecular and morphological analysis of the family Calonymphidae with a description of Calonympha chia sp. nov., Snyderella kirbyi sp. nov., Snyderella swezyae sp. nov. and Snyderella yamini sp. nov. International Journal of Systematic and Evolutionary Microbiology, 61, 2547-2558. Available from: https://doi.org/10.1099/ijs.0.028480-0

Gile, G.H., James, E.R., Tai, V., Harper, J.T., Merrell, T.L., Boscaro, V. et al. (2018) New species of Spirotrichonympha from Reticulitermes and the relationships among genera in Spirotrichonymphea. The Journal of Eukaryotic Microbiology, 65, 159-169. Available from: https://doi.org/10.1111/jeu.12447

Gile, G.H. & Slamovits, C.H. (2012) Phylogenetic position of Lophomonas striata Bütschli (Parabasalia) from the hindgut of the cockroach Periplaneta americana. Protist, 163, 274-283. Available from: https://doi.org/10.1016/j.protis.2011.07.002

Harper, J.T., Gile, G.H., James, E.R., Carpenter, K.J. & Keeling, P.K. (2009) The inadequacy of morphology for species and genus delineation in microbial eukaryotes: an example from the parabasalian termite symbiont Coronympha. PLoS One, 4, e6577. Available from: https://doi.org/10.1371/journal.pone.0006577

James, E.R., Burki, F., Harper, T., Scheffrahn, R.H. & Keeling, P.J. (2013) Molecular characterization of parabasalian symbionts Coronympha clevelandii and Trichonympha subquasilla from the Hawaiian lowland tree termite Incisitermes immigrans. The Journal of Eukaryotic Microbiology, 60, 313-316. Available from: https://doi.org/10.1111/jeu.12027

James, E.R., Tai, V., Scheffrahn, R.H. & Keeling, P.J. (2013) Trichonympha burlesquei n. sp. from Reticulitermes virginicus and evidence against a cosmopolitan distribution of Trichonympha agilis in many termite hosts. International Journal of Systematic and Evolutionary Microbiology, 63, 3873-3876. Available from: https://doi.org/10.1099/ijs.0.054874-0

Janicki, C. (1911) Zur Kenntnis des Parabasalapparats bei parasitischen Flagellaten. Biologisches Centralblatt, 31, 321-330.

Jasso-Selles, D.E., De Martini, F., Velenovsky, J.F., Mee, E.D., Montoya, S.J., Hileman, J.T. et al. (2020) The complete protist symbiont communities of Coptotermes formosanus and Coptotermes gestroi: morphological and molecular characterization of five new species. The Journal of Eukaryotic Microbiology, 67, 626-641. Available from: https://doi.org/10.1111/jeu.12815

Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772-780. Available from: https://doi.org/10.1093/molbev/mst010

Keeling, P.J. (2002) Molecular phylogenetic position of Trichomitopsis termopsidis (Parabasalia) and evidence for the Trichomitopsiinae. European Journal of Protistology, 38, 279-286. Available from: https://doi.org/10.1078/0932-4739-00874

Kirby, H. (1929) Snyderella and Coronympha, two new genera of multinucleate flagellates from termites. University of California Publications in Zoology, 31, 417-432.

Kirby, H. (1939) Two new flagellates from termites in the genera Coronympha Kirby, and Metacoronympha Kirby, new genus. Proceedings of the California Academy of Sciences, 22, 207-220.

Kirby, H. (1947) Flagellate and host relationships of trichomonad flagellates. The Journal of Parasitology, 33, 214-228.

Medlin, L., Elwood, H.J., Stickel, S. & Sogin, M.L. (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71, 491-499. Available from: https://doi.org/10.1016/0378-1119(88)90066-2

Michaud, C., Hervé, V., Dupont, S., Dubreuil, G., Bézier, A.M., Meunier, J. et al. (2019) Efficient but occasionally imperfect vertical transmission of gut mutualistic protists in a wood-feeding termite. Molecular Ecology, 29, 308-324. Available from: https://doi.org/10.1111/mec.15322

Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268-274. Available from: https://doi.org/10.1093/molbev/msu300

Noda, S., Mantini, C., Bordereau, C., Kitade, O., Dolan, M.F., Viscogliosi, E. et al. (2009) Molecular phylogeny of parabasalids with emphasis on the order Cristamonadida and its complex morphological evolution. Molecular Phylogenetics and Evolution, 52, 217-224. Available from: https://doi.org/10.1016/j.ympev.2009.03.011

Noda, S., Mantini, C., Meloni, D., Inoue, J.-I., Kitade, O., Viscogliosi, E. et al. (2012) Molecular phylogeny and evolution of Parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1α. PLoS One, 7, e29938. Available from: https://doi.org/10.1371/journal.pone.0029938

Noda, S., Shimizu, D., Yuki, M., Kitade, O. & Ohkuma, M. (2018) Host-symbiont cospeciation of termite-gut cellulolytic protists of the genera Teranympha and Eucomonympha and their Treponema endosymbionts. Microbes and Environments, 1, 26-33. Available from: https://doi.org/10.1264/jsme2.ME17096

Noël, C., Noda, S., Mantini, C., Dolan, M.F., Moriya, S., Delgado-Viscogliosi, P. et al. (2007) Molecular phylogenetic position of the genera Stephanonympha and Caduceia (Parabasalia) inferred from nuclear small subunit rRNA gene sequences. The Journal of Eukaryotic Microbiology, 54, 93-99. Available from: https://doi.org/10.1111/j.1550-7408.2006.00234.x

Ohkuma, M., Iida, T., Ohtoko, K., Yuzawa, H., Noda, S., Viscogliosi, E. et al. (2005) Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Hypermastigea. Molecular Phylogenetics and Evolution, 35, 646-655. Available from: https://doi.org/10.1016/j.ympev.2005.02.013

Ohkuma, M., Ohtoko, K., Iida, T., Tokura, S., Moriya, S., Usami, R. et al. (2000) Phylogenetic identification of hypermastigotes, Pseudotrichonympha, Spirotrichonympha, Holomastigotoides, and parabasalian symbionts, in the hindgut of termites. The Journal of Eukaryotic Microbiology, 47, 249-259. Available from: https://doi.org/10.1111/j.1550-7408.2000.tb00044.x

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S. et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539-542. Available from: https://doi.org/10.1093/sysbio/sys029

Scheffrahn, R.H. & Carrijo, T.E. (2020) Three new species of Rugitermes (Isoptera, Kalotermitidae) from Peru and Bolivia. ZooKeys, 1000, 31-44. Available from: https://doi.org/10.3897/zookeys.1000.59219

Scheffrahn, R.H., Mullins, A.J., Krecek, J., Chase, J.A., Mangold, J.R., Myles, T. et al. (2015) Global elevation, latitudinal, and climatic limits for termites and the redescription of Rugitermes laticollis Snyder (Isoptera: Kalotermitidae) from the Andean highlands. Sociobiology, 62, 426-438. Available from: https://doi.org/10.13102/sociobiology.v62i3.793

Singh, R.A., Boscaro, V., James, E.R., Karnkowska, A., Kolisko, M., Gavelis, G.S. et al. (2021) Characterization of new cristamonad species from kalotermitid termites including a novel genus, Runanympha. Scientific Reports, 11, 7270. Available from: https://doi.org/10.1038/s41598-021-86645-w

Tamm, S.L. (1978) Laser microbeam study of a rotary motor in termite flagellates. Evidence that the axostyle complex generates torque. The Journal of Cell Biology, 78, 76-92. Available from: https://doi.org/10.1083/jcb.78.1.76

Tamm, S.L. (2008) Unsolved motility looking for an answer. Cell Motility and the Cytoskeleton, 65, 435-440. Available from: https://doi.org/10.1002/cm.20276

Tamm, S.L. & Tamm, S. (1974) Direct evidence for fluid membranes. Proceedings of the National Academy of Sciences of the United States of America, 71, 4589-4593. Available from: https://doi.org/10.1073/pnas.71.11.4589

Tamm, S.L. & Tamm, S. (1976) Rotary movements and fluid membranes in termite flagellates. Journal of Cell Science, 20, 619-639. Available from: https://doi.org/10.1242/jcs.20.3.619

Trager, W. (1934) The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. The Biological Bulletin, 66, 182-190.

Yamin, M.A. (1979) Flagellates of the orders Trichomonadida Kirby, Oxymonadida Grassé, and Hypermastigida Grassi & Foà reported from lower termites (Isoptera families Mastotermitidae, Kalotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae and Serritermitidae) and from the wood-feeding roach Cryptocercus (Dictyoptera: Cryptocercidae). Sociobiology, 4, 3-119.

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