Symbiosis, morphology, and phylogeny of hoplonymphidae (Parabasalia) of the wood-feeding roach cryptocercus punctulatus

Journal of Eukaryotic Microbiology

Volumn 58, Issue 5, 2011, Pages 426-436

  Carpenter, Kevin J ^a,b   Horak, Ales ^a   Chow, Lawrence ^a   Keeling, Patrick J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

Anaerobic protists; flagellates; Hoplonymphidae; morphology; Parabasalia; scanning electron microscopy; symbiosis; termites

Indexed keywords

ANOXIC CONDITIONS; BACTERIUM; CELLULOSE; COCKROACH; CYTOPLASM; EVOLUTIONARY BIOLOGY; FLAGELLATE; LIFE CYCLE; MORPHOLOGY; PHYLOGENETICS; PHYLOGENY; SCANNING ELECTRON MICROSCOPY; SPECIES DIVERSITY; SYMBIOSIS; TERMITE;

ANIMAL; ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; CLASSIFICATION; COCKROACH; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PARABASALIA; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS; WOOD;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; COCKROACHES; MOLECULAR SEQUENCE DATA; PARABASALIDEA; PHYLOGENY; SYMBIOSIS; WOOD;

BACTERIA (MICROORGANISMS); BARBULANYMPHA; BLATTARIA; CRYPTOCERCUS; CRYPTOCERCUS PUNCTULATUS; HOPLONYMPHIDAE; ISOPTERA; MASTIGOPHORA (FLAGELLATES); PARABASALIDEA; PROTISTA;

EID: 80053180572     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2011.00564.x     Document Type: Article

References (45)

1. Bloodgood, R. A., &, Fitzharris, T. P., 1976. Specific associations of prokaryotes with symbiotic flagellate protozoa from the hindgut of the termite Reticulitermes and the wood-eating roach Cryptocercus. Cytobios, 17: 103-122.
2. Brugerolle, G., &, Bordereau, C., 2004. The flagellates of the termite Hodotermopsis sjoestedti with special reference to Hoplonympha, Holomastigotes and Trichomonoides trypanoides n. comb. Eur. J. Protistol., 40: 163-174. (Pubitemid 39040415)
3. Brugerolle, G., &, Lee, J. J., 2000. Phylum Parabasalia. In:, Lee, J. J., Leedale, G. F., &, Bradbury, P., (ed.), An Illustrated Guide to the Protozoa. 2nd ed. Allen Press Inc, Lawrence, KS. 2: 1196-1250.
4. Carpenter, K. J., &, Keeling, P. J., 2007. Morphology and phylogenetic position of Eucomonympha imla (Parabasalia: Hypermastigida). J. Eukaryot. Microbiol., 54: 325-332. (Pubitemid 47174367)
5. 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.
6. Carpenter, K. J., Horak, A., &, Keeling, P. J., 2010. Phylogenetic position and morphology of Spirotrichosomidae (Parabasalia): new evidence from Leptospironympha of Cryptocercus punctulatus. Protist, 161: 122-132.
7. Carpenter, K. J., Waller, R. F., &, Keeling, P. J., 2008. Surface morphology of Saccinobaculus (Oxymonadida): implications for character evolution and function in oxymonads. Protist, 159: 209-221. (Pubitemid 351406511)
8. 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.
9. Cleveland, L. R., 1951. Hormone-induced sexual cycles of flagellates. VII. One-division meiosis and autogamy without cell division in Urinympha. J. Morph., 88: 385-439.
10. Cleveland, L. R., &, Grimstone, A. V., 1964. The fine structure of the flagellate Mixotricha paradoxa and its associated microorganisms. Proc. R. Soc., 159: 668-686.
11. Cleveland, L. R., Hall, S. R., Sanders, E. P., &, Collier, J., 1934. The wood-feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem. Am. Acad. Arts Sci., 17: 1-342.
12. Everaerts, C., Maekawa, K., Farine, J. P., Shimada, K., Luykx, P., Brossut, R., &, Nalepa, C. A., 2008. The Cryptocercus punctulatus species complex (Dictyoptera: Cryptocercidae) in the eastern United States: comparison of cuticular hydrocarbons, chromosome number, and DNA sequences. Mol. Phylogenet. Evol., 47: 950-959.
13. Grassi, B., 1917. Flagellati viventi nei Termiti. Mem. R. Accad. Lincei., 12: 331-394.
14. Hausmann, K., Hülsmann, N., &, Radek, R., 2003. Protistology. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart, Germany.
15. Hollande, A., &, Carruette-Valentin, J., 1971. Les atractophores, l'induction du fuseau et la division cellulaire chez les Hypermastigines Étude infrastructurale et révision systématique desTrichonymphines et des Spirotrichonymphines. Protistologica, 7: 5-100.
16. Hongoh, Y., Sharma, V. K., Prakash, T., Noda, S., Taylor, T. D., Kudo, T., Sakaki, Y., Toyoda, A., Hattori, M., &, Ohkuma, M., 2008a. Complete genome of the uncultured termite group 1 bacteria in a single host protist cell. Proc. Natl. Acad. Sci. USA, 105: 5555-5560. (Pubitemid 351753901)
17. Hongoh, Y., Sharma, V. K., Prakash, T., Noda, S., Toh, H., Taylor, T. D., Kudo, T., Sakaki, Y., Toyoda, A., Hattori, M., &, Ohkuma, M., 2008b. Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science, 322: 1108-1109.
18. Ikeda-Ohtsubo, W., Desai, M., Stingl, U., &, Brune, A., 2007. Phylogenetic diversity of 'Endomicrobia' and their specific affiliation with termite gut flagellates. Microbiology, 153: 3458-3465. (Pubitemid 47629550)
19. Keeling, P. J., 2002. Molecular phylogenetic position of Trichomitopsis termopsidis (Parabasalia) and evidence for the Trichomitopsiinae. Eur. J. Protistol., 38: 279-286. (Pubitemid 35255327)
20. Lartillot, N., Lepage, T., &, Blanquart, S., 2009. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics, 25: 2286-2288.
21. Leidy, J., 1877. On intestinal parasites of Termes flavipes. Proc. Acad. Nat. Sci. Philadelphia, 29: 146-149.
22. Müller, M., 1993. The hydrogenosome. J. Gen. Microbiol., 139: 2879-2889.
23. Nakashima, K. I., Watanabe, H., &, Azuma, J. I., 2002. Cellulase genes from the parabasalian symbiont Pseudotrichonympha grassii in the hindgut of the wood-feeding termite Coptotermes formosanus. Cell. Mol. Life Sci., 59: 1554-1560. (Pubitemid 35239309)
24. Nalepa, C. A., Luykx, P., Klass, K. D., &, Deitz, L. L., 2002. Distribution of karyotypes of the Cryptocercus punctulatus species complex (Dictyoptera: Cryptocercidae) in the Southern Appalachians: relation to habitat and history. Ann. Entomol. Soc. Am., 95: 276-287. (Pubitemid 34718570)
25. Noda, S., Hongoh, Y., Sato, T., &, Ohkuma, M., 2009. Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites. BMC Evol. Biol., 9: 158.
26. Noda, S., Iida, T., Kitade, O., Nakajima, H., Kudo, T., &, Ohkuma, M., 2005. Endosymbiotic Bacteroidales bacteria of the flagellated protist Pseudotrichonympha grassii in the gut of the termite Coptotermes formosanus. Appl. Environ. Microbiol., 71: 8811-8817. (Pubitemid 41804018)
27. Noda, S., Inoue, T., Hongoh, Y., Kawai, M., Nalepa, C. A., Vongkaluang, C., Kudo, T., &, Ohkuma, M., 2006. Identification and characterization of ectosymbionts of distinct lineages in Bacteroidales attached to flagellated protists in the gut of termites and a wood-feeding cockroach. Environ. Microbiol., 8: 11-20.
28. Noda, S., Kitade, O., Inoue, T., Kawai, M., Kanuka, 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. (Pubitemid 46357396)
29. Ohkuma, M., 2008. Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol., 16: 345-352.
30. Ohkuma, M., &, Kudo, T., 1996. Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl. Environ. Microbiol., 62: 461-468. (Pubitemid 26051567)
31. 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. Biol. Sci., 276: 239-245.
32. Radek, R., &, Tischendorf, G., 1999. Bacterial adhesion to different termite flagellates: ultrastructural and functional evidence for distinct molecular attachment modes. Protoplasma, 207: 43-53. (Pubitemid 29319447)
33. Radek, R., Hausmann, K., &, Breunig, A., 1992. Ectobiotic and endocytobiotic bacteria associated with the termite flagellate Joenia-Annectens. Acta Protozoologica, 31: 93-107.
34. Ronquist, F., &, Huelsenbeck, J. P., 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572-1574.
35. Rother, A., Radek, R., &, Hausmann, K., 1999. Characterization of surface structures covering termite flagellates of the family Oxymonadidae and ultrastructure of two oxymonad species, Microrhopalodina multinucleata and Oxymonas sp. Eur. J. Protistol., 35: 1-16. (Pubitemid 29133964)
36. Shimodaira, H., 2002. An approximately unbiased test of phylogenetic tree selection. Syst. Biol., 51: 492-508. (Pubitemid 35180700)
37. Shimodaira, H., &, Hasegawa, M., 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics, 17: 1246-1247. (Pubitemid 33735360)
38. Smith, H. E., &, Arnott, H. J., 1974. Epi- and endobiotic bacteria associated with Pyrsonympha vertens, a symbiotic protozoon of the termite Reticultermes flavipes. Trans. Am. Micros. Soc., 93: 180-194.
39. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22: 2688-2690. (Pubitemid 44642609)
40. Stingl, U., Radek, R., Yang, H., &, Brune, A., 2005. "Endomicrobia": Cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes. Appl. Environ. Microbiol., 71: 1473-1479.
41. Tamm, S. L., 1980. The ultrastructure of prokaryotic-eukaryotic cell junctions. J. Cell. Sci., 44: 335-352. (Pubitemid 10020009)
42. Todaka, N., Inoue, T., Saita, K., Ohkuma, M., Nalepa, C. A., Lenz, M., Kudo, T., &, Moriya, S., 2010. Phylogenetic analysis of cellulolytic enzyme genes from representative lineages of termites and a related cockroach. PLoS One, 5: e8636.
43. Trager, W., 1934. The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol. Bull., 66: 182-190.
44. Yamin, M. A., 1979. Flagellates of the orders Trichomonadida Kirby, Oxymonadida Grasse, and Hypermastigida Grassi and Foa 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.
45. Yamin, M. A., 1980. Cellulose metabolism by the termite flagellate Trichomitopsis termopsidis. Appl. Environ. Microbiol., 39: 859-863. (Pubitemid 10038178)