Identification and localization of the multiple bacterial symbionts of the termite gut flagellate Joenia annectens

Microbiology

Volumn 156, Issue 7, 2010, Pages 2068-2079

  Strassert, Jürgen F H ^a   Desai, Mahesh S ^b   Radek, Renate ^a   Brune, Andreas ^b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL SUBUNIT RIBOSOMAL RNA;

ARTICLE; BACTERIAL GENE; BACTERIUM IDENTIFICATION; BACTEROIDALES; BACTEROIDETES; CELL SURFACE; ENDOSYMBIONT; FLAGELLATE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE SEQUENCE; HOST; INTESTINE; ISOPTERA; JOENIA ANNECTENS; KALOTERMES FLAVICOLLIS; MICROBIAL COLONIZATION; MORPHOTYPE; NITROGEN METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SPIROCHETE; SYMBIONT; ULTRASTRUCTURE; ANIMAL; BACTERIA; BACTERIAL PHENOMENA AND FUNCTIONS; CLASSIFICATION; GASTROINTESTINAL TRACT; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PARABASALIA; PARASITOLOGY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; GASTROINTESTINAL TRACT; ISOPTERA; MOLECULAR SEQUENCE DATA; PARABASALIDEA; PHYLOGENY; SYMBIOSIS;

BACTERIA (MICROORGANISMS); BACTEROIDALES; BACTEROIDETES; EUKARYOTA; ISOPTERA; JOENIA ANNECTENS; KALOTERMES FLAVICOLLIS; MASTIGOPHORA (FLAGELLATES); PROKARYOTA; SPIROCHAETALES;

EID: 77954604506     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.037267-0     Document Type: Article

References (53)

1. Amann, R. I., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R. & Stahl, D. A. (1990). Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56, 1919-1925. (Pubitemid 20202165)
2. Berlanga, M., Paster, B. J. & Guerrero, R. (2007). Coevolution of symbiotic spirochete diversity in lower termites. Int Microbiol 10, 133-139. (Pubitemid 47173985)
3. Brune, A. (2006). Symbiotic associations between termites and prokaryotes. In The Prokaryotes, Symbiotic Associations, Biotechnology, Applied Microbiology, 3rd edn, vol. 1, pp. 439-474. Edited by M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt. New York: Springer.
4. Brune, A. & Stingl, U. (2005). Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis. In Molecular Basis of Symbiosis, pp. 39-60. Edited by J. Overmann. Berlin: Springer.
5. Cleveland, L. R. (1926). Symbiosis among animals with special reference to termites and their intestinal flagellates. Q Rev Biol 1, 51-64.
6. Cleveland, L. R. & Grimstone, A. V. (1964). The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Proc R Soc Lond B Biol Sci 159, 668-686.
7. Desai, M. S., Strassert, J. F. H., Meuser, K., Hertel, H., Ikeda-Ohtsubo, W., Radek, R. & Brune, A. (2009). Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environ Microbiol (Epub ahead of print).
8. Edwards, U., Rogall, T., Blöcker, H., Emde, M. & Böttger, E. C. (1989). Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17, 7843-7853.
9. Fenchel, T. & Ramsing, N. B. (1992). Identification of sulphate-reducing ectosymbiotic bacteria from anaerobic ciliates using 16S rRNA binding oligonucleotide probes. Arch Microbiol 158, 394-397.
10. Fuchs, B. M., Glöckner, F. O., Wulf, J. & Amann, R. (2000). Unlabeled helper oligonucleotides increase the in situ accessibility to 16S rRNA of fluorescently labeled oligonucleotide probes. Appl Environ Microbiol 66, 3603-3607. (Pubitemid 30624603)
11. Geissinger, O., Herlemann, D. P. R., Mörschel, E., Maier, U. G. & Brune, A. (2009). The ultramicrobacterium "Elusimicrobium minutum" gen. nov., sp. nov., the first cultivated representative of the Termite Group 1 phylum. Appl Environ Microbiol 75, 2831-2840.
12. Gold, K. & Pollinger, U. (1971). Occurrence of endosymbiotic bacteria in marine dinoflagellates. J Phycol 7, 264-265.
13. Hongoh, Y., Sato, T., Dolan, M. F., Noda, S., Ui, S., Kudo, T. & Ohkuma, M. (2007a). The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the "Synergistes" group. Appl Environ Microbiol 73, 6270-6276.
14. Hongoh, Y., Sato, T., Noda, S., Ui, S., Kudo, T. & Ohkuma, M. (2007b). Candidatus Symbiothrix dinenymphae: bristle-like Bacteroidales ectosymbionts of termite gut protists. Environ Microbiol 9, 2631-2635. (Pubitemid 47366659)
15. 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 U S A 105, 5555-5560. (Pubitemid 351753901)
16. Hongoh, Y., Sharma, V. K., Prakash, T., Noda, S., Toh, H., Taylor, T. D., Kudo, T., Sakaki, Y., Toyoda, A. & other authors (2008b). Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322, 1108-1109.
17. Hungate, R. E. (1955). Mutualistic intestinal protozoa. In Biochemistry and Physiology of Protozoa, vol. 2, pp. 159-199. Edited by S. H. Hutner & A. Lwoff. New York: Academic Press.
18. Ikeda-Ohtsubo, W. (2007). Endomicrobia in termite guts: symbionts within a symbiont. Phylogeny, cospeciation with host flagellates, and preliminary genome analysis. Dissertation, Philipps-Universität Marburg, Germany.
19. Ikeda-Ohtsubo, W. & Brune, A. (2009). Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and 'Candidatus Endomicrobium trichonymphae'. Mol Ecol 18, 332-342.
20. 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)
21. Ikeda-Ohtsubo, W., Faivre, N. & Brune, A. (2010). Putatively free-living "Endomicrobia" - ancestors of the intracellular symbionts of termite gut flagellates? Environ Microbiol Rep, doi:10.1111/j.1758-2229.2009. 00124.x.
22. Inoue, T., Kitade, O., Yoshimura, T. & Yamaoka, I. (2000). Symbiotic associations with protists. In Termites: Evolution, Sociality, Symbioses, Ecology, pp. 275-288. Edited by T. Abe, D. E. Bignell & M. Higashi. Dordrecht: Kluwer.
23. Kirby, H. (1964). Organisms living on and in protozoa. In Protozoa in Biological Research, pp. 1009-1113. Edited by G. N. Calkins & F. M. Summers. New York: Hafner Publishing Co.
24. Lilburn, T. G., Schmidt, T. M. & Breznak, J. A. (1999). Phylogenetic diversity of termite gut spirochaetes. Environ Microbiol 1, 331-345. (Pubitemid 129640110)
25. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S. & other authors (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32, 1363-1371. (Pubitemid 38854737)
26. Manz, W., Amann, R., Ludwig, W., Vancanneyt, M. & Schleifer, K.-H. (1996). Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142, 1097-1106.
27. Noda, S., Ohkuma, M., Yamada, A., Hongoh, Y. & Kudo, T. (2003). Phylogenetic position and in situ identification of ectosymbiotic spirochetes on protists in the termite gut. Appl Environ Microbiol 69, 625-633.
28. Noda, S., Inoue, T., Hongoh, Y., Kawai, M., Nalepa, C. A., Vongkaluang, C., Kudo, T. & Ohkuma, M. (2006a). 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.
29. Noda, S., Kawai, M., Nakajima, H., Kudo, T. & Ohkuma, M. (2006b). Identification and in situ detection of two lineages of Bacteroidales ectosymbionts associated with a termite gut protist, Oxymonas sp. Microbes Environ 20, 16-22.
30. Noda, S., Kitade, O., Inoue, T., Kawai, M., Kanuka, M., Hiroshima, K., Hongoh, Y., Constantino, R., Uys, V. & other authors (2007). Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol Ecol 16, 1257-1266.
31. 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.
32. Ohkuma, M. (2008). Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16, 345-352.
33. Ohkuma, M., Ohtoko, K., Grunau, C., Moriya, S. & Kudo, T. (1998). Phylogenetic identification of the symbiotic hypermastigote Trichonympha agilis in the hindgut of the termite Reticulitermes speratus based on small-subunit rRNA sequence. J Eukaryot Microbiol 45, 439-444.
34. Ohkuma, M., Iida, T. & Kudo, T. (1999). Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites. FEMS Microbiol Lett 181, 123-129. (Pubitemid 29516611)
35. Ohkuma, M., Noda, S., Hongoh, Y. & Kudo, T. (2002). Diverse bacteria related to the Bacteroides subgroup of the CFB phylum within the gut symbiotic communities of various termites. Biosci Biotechnol Biochem 66, 78-84. (Pubitemid 39251091)
36. Ohkuma, M., Sato, T., Noda, S., Ui, S., Kudo, T. & Hongoh, Y. (2007). The candidate phylum 'Termite Group 1' of bacteria: phylogenetic diversity, distribution, and endosymbiont members of various gut flagellated protists. FEMS Microbiol Ecol 60, 467-476.
37. Radek, R. (1999). Flagellates, bacteria, and fungi associated with termites: diversity and function in nutrition - a review. Ecotropica 5, 183-196.
38. Radek, R., Hausmann, K. & Breunig, A. (1992). Ectobiotic and endocytobiotic bacteria associated with the termite flagellate Joenia annectens. Acta Protozool 31, 93-107.
39. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208-212.
40. Sato, T., Hongoh, Y., Noda, S., Hattori, S., Ui, S. & Ohkuma, M. (2009). Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut. Environ Microbiol 11, 1007-1015.
41. Schweikert, M. & Meyer, B. (2001). Characterization of intracellular bacteria in the freshwater dinoflagellate Peridinium cinctum. Protoplasma 217, 177-184. (Pubitemid 32657033)
42. Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26, 31-43.
43. 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. (Pubitemid 36684414)
44. Stingl, U., Maass, 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.
45. 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.
46. Strassert, J. F. H., Desai, M. S., Brune, A. & Radek, R. (2009). The true diversity of devescovinid flagellates in the termite Incisitermes marginipennis. Protist 160, 522-535.
47. Tamm, S. L. (1982). Flagellated ectosymbiotic bacteria propel a eucaryotic cell. J Cell Biol 94, 697-709.
48. Tanner, A. C. R., Listgarten, M. A., Ebersole, J. L. & Strzempko, M. N. (1986). Bacteroides forsythus sp. nov., a slow-growing, fusiform, Bacteroides sp. from human oral cavity. Int J Syst Bacteriol 36, 213-221.
49. Trager, W. (1934). The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol Bull 66, 182-190.
50. Wallner, G., Amann, R. & Beisker, W. (1993). Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14, 136-143. (Pubitemid 23042736)
51. Warnecke, F., Luginbühl, P., Ivanova, N., Ghassemian, M., Richardson, T. H., Stege, J. T., Cayouette, M., McHardy, A. C., Djordjevic, G. & other authors (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560-565.
52. Weisburg, W. G., Barns, S. M., Pelletier, D. A. & Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697-703.
53. Wenzel, M., Radek, R., Brugerolle, G. & König, H. (2003). Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. Eur J Protistol 39, 11-23. (Pubitemid 36684416)