Ectobiotic spirochetes of flagellates from the termite Mastotermes darwiniensis: Attachment and cyst formation

European Journal of Protistology

Volumn 43, Issue 4, 2007, Pages 281-294

  Radek, Renate ^a   Nitsch, Gülcan ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Deltotrichonympha; Mastotermes darwiniensis; Mixotricha paradoxa; Parabasalids; Spirochete cyst; Termite

Indexed keywords

BACTERIA (MICROORGANISMS); DELTOTRICHONYMPHA; ISOPTERA; MASTIGOPHORA (FLAGELLATES); MASTOTERMES DARWINIENSIS; MIXOTRICHA; MIXOTRICHA PARADOXA; PARABASALIDEA; SPIROCHAETALES;

EID: 35148870567     PISSN: 09324739     EISSN: 16180429     Source Type: Journal    
DOI: 10.1016/j.ejop.2007.06.004     Document Type: Article

References (59)

1. Bloodgood R.A., and Fitzharris T.P. Specific associations of prokaryotes with symbiotic flagellate protozoa from the hindgut of the termite Reticulitermes and the wood-eating roach Cryptocercus. Cytobios 17 (1976) 103-122
2. Branton D., Bullivant S., Gilula N.B., Karnovsky M.J., Moor H., Mühlethaler K., Northcote D.H., Packer L., Satir B., Satir P., Speth V., Staehlin L.A., Steere R.L., and Weinstein R.S. Freeze-etching nomenclature. Science, NY 190 (1975) 54-56
3. Breinl A. On the morphology and life history of Spirochaeta duttoni. Ann. Trop. Med. Parasitol. 1 (1907) 435-438
4. Breznak J.A. Phylogenetic diversity and physiology of termite gut spirochetes. Integr. Comp. Biol. 42 (2002) 313-318
5. Brorson Ø., and Brorson S.-H. Transformation of cystic forms of Borrelia burgdorferi to normal, mobile spirochetes. Infection 25 (1997) 240-246
6. Brorson Ø., and Brorson S.-H. A rapid method for generating cystic forms of Borrelia burgdorferi, and their reversal to mobile spirochetes. Acta Path. Microbiol. Immunol. Scand 106 (1998) 1131-1141
7. Brorson Ø., and Brorson S.-H. In vitro conversion of Borrelia burgdorferi to cystic forms in spinal fluid, and transformation to mobile spirochetes by incubation in BSK-H medium. Infection 26 (1998) 144-149
8. Brugerolle G. Devescovinid features, a remarkable surface cytoskeleton, and epibiotic bacteria revisited in Mixotricha paradoxa, a parabasalid flagellate. Protoplasma 224 (2004) 49-59
9. Brune A., and Stingl U. Prokaryotic symbionts of termite gut flagellates, phylogenetic and metabolic implications of a tripartite symbiosis. In: Overmann J. (Ed). Molecular Basis of Symbiosis (2005), Springer, Berlin 39-60
10. Cleveland L.R. General features of the flagellate and ameboid stages of Deltotrichonympha operculata and D. nana, sp. nov. Arch. Protistenkd 109 (1966) 1-7
11. Cleveland L.R. General features and reproduction in Koruga bonita gen. et sp. nov. Arch. Protistenkd. 109 (1966) 18-23
12. Cleveland L.R., and Cleveland B.T. The locomotory waves of Koruga, Deltotrichonympha, and Mixotricha. Arch. Protistenkd. 109 (1966) 39-63
13. Cleveland L.R., and Grimstone A.V. The fine structure of the flagellate Mixotricha paradoxa and its associated microorganisms. Proc. R. Soc. London, Ser. B 159 (1964) 668-686
14. Dexter Dyer B., and Khalsa O. Surface bacteria of Streblomastix strix are sensory symbionts. Biosystems 31 (1993) 169-180
15. Dolan M.F., Wier A.M., Melnitsky H., Whiteside J.H., and Margulis L. Cysts and symbionts of Staurojoenina assimilis Kirby from Neotermes. Eur. J. Protistol. 40 (2004) 257-264
16. Dorward D.W., and Garon C.F. DNA is packaged within membrane-derived vesicles of gram-negative but not gram-positive bacteria. Appl. Environ. Microbiol. 56 (1990) 1960-1962
17. Doyle R.J. Strategies in experimental microbial adhesion research. In: Mozes N., Handley P.S., Busscher H.J., and Rouxhet P.G. (Eds). Microbial Cell Surface Analysis. Structural and Physicochemical Methods (1991), VCH Publishers, Inc., New York 291-316
18. Dröge S., Fröhlich J., Radek R., and König H. Spirochaeta coccoides, a novel coccoid spirochete from the hindgut of the termite Neotermes castaneus. Appl. Environ. Microbiol. 72 (2006) 392-397
19. Fröhlich J., and König H. Rapid isolation of single microbial cells from mixed natural and laboratory populations with the aid of a micromanipulator. Syst. Appl. Microbiol. 22 (1999) 249-257
20. Garon C.F., Dorward D.W., and Corwin M.D. Structural features of Borrelia burgdorferi - the Lyme disease spirochete: silver staining for nucleic acids. Scan. Microsc. Suppl. 3 (1989) 109-115
21. Gruntar I., Malovrh T., Murgia R., and Cinco M. Conversion of Borrelia garinii cystic forms to motile spirochetes in vivo. Acta Path. Microbiol. Immunol. Scand. 109 (2001) 383-388
22. Guerrero R., Ashen J., Solé M., and Margulis L. Spirosymplokos deltaeiberi nov. gen., nov. sp., variable-diameter composite spirochete from microbial mats. Arch. Microbiol. 160 (1993) 461-470
23. Hampp E.G., and Bethesda M.S. Morphologic characteristics of the smaller oral treponemes and Borrelia vincentii as revealed by stained smear, darkfield and electron microscopic technics. J. Amer. Dent. Ass. 40 (1950) 1-11
24. Hugenholtz P., Goebel B.M., and Pace N.R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180 (1998) 4765-4774
25. Hulínská D., Bartak P., Hercogová J., Hancil J., Basta J., and Schramlová J. Electron microscopy of Langerhans cells and Borrelia burgdorferi in Lyme disease patients. Zbl. Bakt. 280 (1994) 348-359
26. Iida T., Ohkuma M., Ohtoko K., and Kudo T. Symbiotic spirochetes in the termite hindgut, phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiol. Ecol. 34 (2000) 16-17
27. König H., Fröhlich J., Li L., Wenzel M., Dröge S., Breunig A., Pfeiffer P., Radek R., and Brugerolle G. The flagellates of the Australian termite Mastotermes darwiniensis, identification of their symbiotic bacteria and cellulases. Symbiosis 44 (2007) 51-65
28. Leander B.S., and Keeling P.J. Symbiotic innovation in the oxymonad Streblomastix strix. J. Eukaryot. Microbiol. 51 (2004) 291-300
29. Lee M.J., Schreurs P.J., Messer A.C., and Zinder S.H. Association of methanogenic bacteria with flagellated protozoa from a termite hindgut. Curr. Microbiol. 15 (1987) 337-341
30. Lilburn T.G., Schmidt T.M., and Breznak J.A. Phylogenetic diversity of termite gut spirochetes. Environ. Microbiol. 1 (1999) 331-345
31. Luft J.H. Ruthenium red and violet, I. Chemistry, purification, methods of use for electron microscopy and mechanisms of action. Anat. Rec. 171 (1971) 347-368
32. Margulis L. Spirochetes. In: Lederberg J., Alexander M., Bloom B., Hopwood D., Hull R., Iglewski B., Laskin A., Oliver S., Schaechter M., and Summers W. (Eds). Encyclopedia of Microbiology vol. 4 (2000), Academic Press, New York 353-363
33. Margulis L., To L.P., and Chase D.G. The genera Pillotina, Hollandina and Diplocalyx. In: Starr M.P., Stolp H., Trüper H.G., Balows A., and Schlegel H.G. (Eds). The Prokaryotes vol. 1 (1981), Springer, Berlin 548-554
34. Murgia R., and Cinco M. Induction of cystic forms by different stress conditions in Borrelia burgdorferi. Acta Path. Microbiol. Immunol. Scand 112 (2004) 57-62
35. Nilsson J. Tetrahymena in cytotoxicology, with special reference to effects of heavy metals and selected drugs. Eur. J. Protistol. 25 (1989) 2-25
36. Noda S., Ohkuma M., Yamada A., Hongoh Y., and Kudo T. Phylogenetic position and in situ identification of ectosymbiotic spirochetes on protists in the termite gut. Appl. Environ. Microbiol. 69 (2003) 625-633
37. Noda S., Iida T., Kitade O., Nakajima H., Kudo T., and Ohkuma M. Endosymbiotic Bacteroidales bacteria of the flagellated protist Pseudotrichonympha grassii in the gut of the termite Coptotermes formosanus. Appl. Environ. Microbiol. 71 (2005) 8811-8817
38. Noda S., Inoue T., Hongoh Y., Kawai M., Nalepa C.A., Vongkaluang C., Kudo T., and Ohkuma M. 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 (2006) 11-20
39. Ohkuma M., and Kudo T. Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl. Environ. Microbiol. 62 (1996) 461-468
40. Ohkuma M., Iida T., and Kudo T. Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites. FEMS Microbiol. Lett. 181 (1999) 123-129
41. Paster B.J., Dewhirst F.E., Cooke S.M., Fussing V., Poulsen L.K., and Breznak J.A. Phylogeny of not-yet-cultured spirochetes from termite guts. Appl. Environ. Microbiol. 62 (1996) 347-352
42. Radek R., and Tischendorf G. Bacterial adhesion to different termite flagellates, ultrastructural and functional evidence for distinct molecular attachment modes. Protoplasma 207 (1999) 43-53
43. Radek R., Hausmann K., and Breunig A. Ectobiotic and endocytobiotic bacteria associated with the termite flagellate Joenia annectens. Acta Protozoologica 31 (1992) 93-107
44. Radek R., Hausmann K., and Haarhaus D. Symbiotic flagellates in termites. Video C 1790 (1992) Vol. 21 (1994), Institute for the Scientific Film, Publ. Sci. Film Biology, Göttingen pp. 153-171
45. Radek R., Roesel J., and Hausmann K. Light and electron microscopic study of the bacterial adhesion to termite flagellates applying lectin cytochemistry. Protoplasma 193 (1996) 105-122
46. Smith H.E., and Arnott H.J. Epi- and endobiotic bacteria associated with Pyrsonympha vertens, a symbiotic protozoon of the termite Reticulitermes flavipes. Trans. Am. Micr. Soc. 93 (1974) 180-194
47. Smith H.E., Buhse H.E., and Stammler S.J. Possible formation and development of spirochaete attachment sites found on the surface of symbiotic polymastigote flagellates of the termite Reticulitermes flavipes. Biosystems 7 (1975) 374-379
48. Stingl U., Maaß A., Radek R., and Brune A. 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 (2004) 2229-2235
49. Stingl U., Radek R., Yang H., and Brune A. "Endomicrobia", cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes. Appl. Environ. Microbiol. 71 (2005) 1473-1479
50. Sutherland J.L. Protozoa from Australian termites. Quart. J. Microsc. Sci. 76 (1933) 145-173
51. Tamm S.L. The ultrastructure of prokaryotic-eukaryotic cell junctions. J. Cell Sci. 44 (1980) 335-352
52. Tamm S.L. Flagellated ectosymbiotic bacteria propel a eukaryotic cell. J. Cell Biol. 94 (1982) 697-709
53. Tamm S., and Tamm S.L. The fine structure of the centriolar apparatus and associated structures in the flagellates Deltotrichonympha and Koruga. I. Interphase. J. Protozool. 20 (1973) 230-245
54. Tokura M., Ohkuma M., and Kudo T. Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites. FEMS Microbiol. Ecol. 33 (2000) 233-240
55. Umemoto T., and Namikawa I. Electron microscopy of the spherical body of oral spirochetes in vitro. Further studies. Microbiol. Immunol. 24 (1980) 321-334
56. Wenzel M., Radek R., Brugerolle G., and König H. Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. Eur. J. Protistol. 39 (2003) 11-23
57. Wier A., Ashen J., and Margulis L. Canaleparolina darwiniensis, gen. nov., sp. nov., and other pillotinaceous spirochetes from insects. Int. Microbiol. 3 (2000) 213-223
58. Wolf V., Lange R., and Wecke J. Development of quasi-multicellular bodies of Treponema denticola. Arch. Microbiol. 160 (1993) 206-213
59. Wood E.J., Seviour R.J., Siddique A.B., Glaisher R.W., Webb R.I., and Trott D.J. Spherical body formation in the spirochaete Brachyspira hyodysenteriae. FEMS Microbiol. Lett. 259 (2006) 14-19