Morphology and molecular phylogeny of staurojoenina mulleri sp. nov. (trichonymphida, parabasalia) from the hindgut of the kalotermitid neotermes jouteli

Journal of Eukaryotic Microbiology

Volumn 60, Issue 2, 2013, Pages 203-213

  Gile, Gillian H ^a,c   Carpenter, Kevin J ^a,d   James, Erick R ^a   Scheffrahn, Rudolf H ^b   Keeling, Patrick J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF FLORIDA   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

^d LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

Barcoding; epibiont; hypermastigote; symbiont; termite

Indexed keywords

PROTOZOAL DNA; PROTOZOAL RNA; RIBOSOME DNA; RIBOSOME RNA; RNA, RIBOSOMAL, 26S;

BACTERIUM; MOLECULAR ANALYSIS; MORPHOLOGY; PHYLOGENETICS; PHYLOGENY; PROTIST; SYMBIONT; TAXONOMY; TERMITE;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; CYTOLOGY; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; ISOPTERA; MICROSCOPY; MOLECULAR GENETICS; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PARABASALIA; PARASITOLOGY; PHYLOGENY; RNA GENE;

ANIMALS; CLUSTER ANALYSIS; DNA, PROTOZOAN; DNA, RIBOSOMAL; GENES, RRNA; ISOPTERA; MICROSCOPY; MOLECULAR SEQUENCE DATA; NORTH AMERICA; PARABASALIDEA; PHYLOGENY; RNA, PROTOZOAN; RNA, RIBOSOMAL; SEQUENCE ANALYSIS, DNA;

BACTERIA (MICROORGANISMS); EUKARYOTA; HYPERMASTIGIA; INCISITERMES MINOR; ISOPTERA; KALOTERMITIDAE; NEOTERMES JOUTELI; PARABASALIDEA; STAUROJOENINA; STAUROJOENINA ASSIMILIS; TRICHONYMPHIDA;

EID: 84874680535     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/jeu.12024     Document Type: Article

References (46)

1. Banks, N., &, Snyder, T. E., 1920. A revision of the Nearctic termites with notes on biology and geographic distribution. Bull. U.S. Nat. Hist. Mus. Wash., 108: 1-228.
2. Capella-Gutiérrez, S., Silla-Martínez, J. M., &, Gabaldõn, T., 2009. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25: 1972-1973.
3. Carpenter, K. J., Chow, L., &, Keeling, P. J., 2009. Morphology, phylogeny, and diversity of Trichonympha (Parabasalia: Hypermastigida) of the wood-feeding cockroach Cryptocercus punctulatus. J. Eukaryot. Microbiol., 56: 305-313.
4. Castresana, J., 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol., 17: 540-552.
5. 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.
6. Cepicka, I., Kutišova, K., Tachezy, J., Kulda, J., &, Flegr, J., 2005. Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Vet. Parasitol., 128: 11-21.
7. Desai, M. S., Strassert, J. F. H., Meuser, K., Hertel, H., Ikeda-Ohtsubo, W., Radek, R., &, Brune, A., 2010. Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environ. Microbiol., 12: 2120-2132.
8. Dolan, M., &, Margulis, L., 1997. Staurojoenina and other symbionts in Neotermes from San Salvador Island, Bahamas. Symbiosis, 22: 229-239.
9. Dolan, M. F., Wier, A. M., Melnitsky, H., Whiteside, J. H., &, Margulis, L., 2004. Cysts and symbionts of Staurojoenina assimilis Kirby from Neotermes. Eur. J. Protistol., 40: 257-264.
10. Gerbod, D., Sanders, E., Moriya, S., Noël, C., Takasu, H., Fast, N. M., Delgado-Viscogliosi, P., Ohkuma, M., Kudo, T., Capron, M., Palmer, J. D., Keeling, P. J., &, Viscogliosi, E., 2004. Molecular phylogenies of Parabasalia inferred from four protein genes and comparison with rRNA trees. Mol. Phylogenet. Evol., 31: 572-580.
11. 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. Int. J. Syst. Evol. Microbiol., 61: 2547-2558.
12. Gouy, M., Guindon, S., &, Gascuel, O., 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol., 27: 221-224.
13. Grassé, P.-P., &, Hollande, A., 1942. Sur la structure des Hypermastigines du genre Staurojoenina. C. R. Acad. Sci., 114: 920-922.
14. Grassé, P.-P., &, Hollande, A., 1945. La structure d'une hypermastigide complexe Staurojoenina caulleryi. Ann. Sci. Nat. Zool. Biol. Anim., 11: 147-165.
15. Grassi, B., 1917. Flagellati viventi nei termiti. Atti Della R. Academia dei Lincei-Memorie Della Classe di Scienze Fisiche Mathematiche e Naturali, 12: 331-394.
16. Hampl, V., Cepicka, I., Flegr, J., Tachezy, J., &, Kulda, J., 2007. Morphological and molecular diversity of the monocercomonadid genera Monocercomonas, Hexamastix, and Honigbergiella gen. nov. Protist, 158: 365-383.
17. Harper, J. T., Gile, G. H., James, E. R., Carpenter, K. J., &, Keeling, P. J., 2009. The inadequacy of morphology for species and genus delineation in microbial eukaryotes: an example from the parabasalian termite symbiont Coronympha. PLoS ONE, 4: e6557.
18. Hollande, A., 1986. Les hypermastigines du genre Staurojoenina. Précisions sur la structure de leur rostre et description d'espèces nouvelles. Protistologica, 22: 331-338.
19. Ikeda-Ohtsubo, W., &, Brune, A., 2009. Cospeciation of termite gut flagellates and their bacterial symbionts: Trichonympha species and 'Candidatus Endomicrobium trichonymphae'. Mol. Ecol., 18: 332-342.
20. Kambhampati, S., &, Smith, P. T., 1995. PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol. Biol., 4: 233-236.
21. Katoh, K., &, Toh, H., 2010. Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics, 26: 1899-1900.
22. Kirby, H., 1926. On Staurojoenia assimilis sp. nov., an intestinal flagellate from the termite, Kalotermes minor Hagen. Univ. Calif. Publ. Zool., 29: 25-102.
23. Light, S. F., &, Sanford, M. F., 1928. Experimental transfaunation of termites. Univ. Calif. Publ. Zool., 31: 269-274.
24. Maa, A., &, Radek, R., 2006. The gut flagellate community of the termite Neotermes cubanus with special reference to Staurojoenina and Trichocovina hrdyi nov. gen. nov. sp. Eur. J. Protistol., 42: 125-141.
25. Moriya, S., Dacks, J. B., Takagi, A., Noda, S., Ohkuma, M., Doolittle, W. F., &, Kudo, T., 2003. Molecular phylogeny of three oxymonad genera: Pyrsonympha, Dinenympha and Oxymonas. J. Eukaryot. Microbiol., 50: 190-197.
26. Noda, S., Kitade, O., Inoue, T., Kawai, M., Hiroshima, K., Hongoh, Y., Constantino, R., Uys, V., Zhong, J., Kudo, T., &, Ohkuma, M., 2007. Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol. Ecol., 16: 1257-1266.
27. Noda, S., Mantini, C., Meloni, D., Inoue, J.-I., Kidade, O., Viscogliosi, E., &, Ohkuma, M., 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.
28. Ohkuma, M., Iida, T., Ohtoko, K., Yuzawa, H., Noda, S., Viscogliosi, E., &, Kudo, T., 2005. Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Hypermastigea. Mol. Phylogenet. Evol., 35: 646-655.
29. Ohkuma, M., Saita, K., Inoue, T., &, Kudo, T., 2007. Comparison of four protein phylogeny of parabasalian symbionts in termite guts. Mol. Phylogenet. Evol., 42: 847-853.
30. Ohkuma, M., Noda, S., Hongoh, Y., Nalepa, C. A., &, Inoue, T., 2009. Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc. R. Soc. Lond., Ser. B: Biol. Sci., 276: 239-245.
31. Posada, D., &, Crandall, K. A., 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics, 14: 817-818.
32. Ronquist, F., &, Huelsenbeck, J. P., 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572-1574.
33. Saldarriaga, J. F., Gile, G. H., James, E. R., Horák, A., Scheffrahn, R. H., &, Keeling, P. J., 2011. Morphology and molecular phylogeny of Pseudotrichonympha hertwigi and Pseudotrichonympha paulistana (Trichonymphea, Parabasalia) from neotropical rhinotermitids. J. Eukaryot. Microbiol., 58: 487-496.
34. Scheffrahn, R. H., Krecek, J., &, Su, N.-Y., 2000. Redescriptions of the Dampwood Termites Neotermes jouteli and N. luykxi (Isoptera: Kalotermitidae) from Florida, Cuba, Bahamas, and Turks and Caicos Islands. Ann. Entomol. Soc. Am., 93: 785-794.
35. Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., &, Flook, P., 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am., 87: 651-701.
36. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22: 2688-2690.
37. Stingl, U., &, Brune, A., 2003. Phylogenetic diversity and whole-cell hybridization of oxymonad flagellates from the hindgut of the wood-feeding lower termite Reticulitermes flavipes. Protist, 154: 147-155.
38. Stingl, U., Maa, A., Radek, R., &, Brune, A., 2004. Symbionts of the gut flagellate Staurojoenina sp. from Neotermes cubanus represent a novel, termite-associated lineage of Bacteroidales: description of 'Candidatus Vestibaculum illigatum'. Microbiology, 150: 2229-2235.
39. Sutherland, J. L., 1933. Protozoa from Australian termites. Q. J. Microsc. Sci., 76: 145-173.
40. Swofford, D. L., 2003. PAUP*. Phylogenetic Analysis Using Parsimony (and Other Methods), 4th ed. Sinauer Associates, Sunderland, Massachusetts.
41. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., &, Higgins, D. G., 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25: 4876-4882.
42. Trager, W., 1934. The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol. Bull., 66: 182-190.
43. Wier, A. M., Dolan, M. F., &, Margulis, L., 2004. Cortical symbionts and hydrogenosomes of the amitochondriate protist Staurojoenina assimilis. Symbiosis, 36: 153-168.
44. Wirth, T., Le Guellec, R., &, Veuille, M., 1999. Directional substitution and evolution of nucleotide content in the cytochrome oxidase II gene in earwigs (dermapteran insects). Mol. Biol. Evol., 16: 1645-1653.
45. 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: 1-120.
46. Yubuki, N., Céza, V., Cepicka, I., Yabuki, A., Inagaki, Y., Nakayama, T., Inouye, I., &, Leander, B. S., 2010. Cryptic diversity of free-living parabasalids, Pseudotrichomonas keilini and Lacusteria cypriaca n. g., n. sp., as inferred from small subunit rDNA sequences. J. Eukaryot. Microbiol., 57: 554-561.