Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut

Environmental Microbiology

Volumn 11, Issue 4, 2009, Pages 1007-1015

  Sato, Tomoyuki ^a,b   Hongoh, Yuichi ^a   Noda, Satoko ^a   Hattori, Satoshi ^a,c   Ui, Sadaharu ^b   Ohkuma, Moriya ^a  

^a RIKEN   (Japan)

^b UNIVERSITY OF YAMANASHI   (Japan)

^c YAMAGATA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIAL RNA; RIBOSOME DNA; RNA 16S;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; DESULFOVIBRIO; DNA SEQUENCE; FLAGELLATE; FLUORESCENCE IN SITU HYBRIDIZATION; GASTROINTESTINAL TRACT; GENETICS; ISOLATION AND PURIFICATION; ISOPTERA; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; RNA GENE; SEQUENCE HOMOLOGY; SYMBIOSIS;

ANIMALS; BACTERIAL PROTEINS; DESULFOVIBRIO; DNA, BACTERIAL; DNA, RIBOSOMAL; GASTROINTESTINAL TRACT; GENES, RRNA; IN SITU HYBRIDIZATION, FLUORESCENCE; ISOPTERA; MASTIGOPHORA; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SYMBIOSIS;

BACTERIA (MICROORGANISMS); COCCOIDEA; DESULFOVIBRIO; ISOPTERA; MASTIGOPHORA (FLAGELLATES); PROKARYOTA; RETICULITERMES SPERATUS; TRICHONYMPHA AGILIS;

EID: 63849272877     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2008.01827.x     Document Type: Article

References (41)

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.
2. Brune, A. Friedrich, M. (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3 : 263 269.
3. Brune, A. Stingl, U. (2006) Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis. Prog Mol Subcell Biol 41 : 39 60.
4. Cline, J.D. (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14 : 454 458.
5. Cypionka, H. (2000) Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54 : 827 848.
6. Dröge, S., Limper, U., Emtiazi, F., Schönig, I., Pavlus, N., Drzyzga, O., et al. (2005) In vitro and in vivo sulfate reduction in the gut contents of the termite Mastotermes darwiniensis and the rose-chafer Pachnoda marginata. J Gen Appl Microbiol 51 : 57 64.
7. Fisher, M., Miller, D., Brewster, C., Husseneder, C. Dickerman, A. (2007) Diversity of gut bacteria of Reticulitermes flavipes as examined by 16S rRNA gene sequencing and amplified rDNA restriction analysis. Curr Microbiol 55 : 254 259.
8. Friedrich, M.W. (2002) Phylogenetic analysis reveals multiple lateral transfers of adenosine-5′-phosphosulfate reductase genes among sulfate-reducing microorganisms. J Bacteriol 184 : 278 289.
9. Fröhlich, J., Sass, H., Babenzien, H.D., Kuhnigk, T., Varma, A., Saxena, S., et al. (1999) Isolation of Desulfovibrio intestinalis sp. nov. from the hindgut of the lower termite Mastotermes darwiniensis. Can J Microbiol 45 : 145 152.
10. Guindon, S. Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 : 696 704.
11. Heidelberg, J.F., Seshadri, R., Haveman, S.A., Hemme, C.L., Paulsen, I.T., Kolonay, J.F., et al. (2004) The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22 : 554 559.
12. Hongoh, Y., Ohkuma, M. Kudo, T. (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44 : 231 242.
13. Hongoh, Y., Deevong, P., Inoue, T., Moriya, S., Trakulnaleamsai, S., Ohkuma, M., et al. (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71 : 6590 6599.
14. Hongoh, Y., Ekpornprasit, L., Inoue, T., Moriya, S., Trakulnaleamsai, S., Ohkuma, M., et al. (2006a) Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol Ecol 15 : 505 516.
15. Hongoh, Y., Deevong, P., Hattori, S., Inoue, T., Noda, S., Noparatnaraporn, N., et al. (2006b) Phylogenetic diversity, localization, and cell morphologies of members of the candidate phylum TG3 and a subphylum in the phylum Fibrobacteres, recently discovered bacterial groups dominant in termite guts. Appl Environ Microbiol 72 : 6780 6788.
16. Hongoh, Y., Sato, T., Noda, S., Ui, S., Kudo, T. Ohkuma, M. (2007a) Candidatus Symbiothrix dinenymphae: bristle-like Bacteroidales ectosymbionts of termite gut protists. Environ Microbiol 9 : 2631 2635.
17. Hongoh, Y., Sato, T., Dolan, M.F., Noda, S., Ui, S., Kudo, T. Ohkuma, M. (2007b) The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the 'Synergistes' group. Appl Environ Microbiol 73 : 6270 6276.
18. Hongoh, Y., Sharma, V.K., Prakash, T., Noda, S., Taylor, T.D., Kudo, T., et al. (2008) Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci USA 105 : 5555 5560.
19. Inoue, J., Saita, K., Kudo, T., Ui, S. Ohkuma, M. (2007) Hydrogen production by termite gut protists: characterization of iron hydrogenases of parabasalian symbionts of the termite Coptotermes formosanus. Eukaryot Cell 6 : 1925 1932.
20. Kent, H.M., Buck, M. Evans, D.J. (1989) Cloning and sequencing of the nifH gene of Desulfovibrio gigas. FEMS Microbiol Lett 52 : 73 78.
21. Kirby, H. (1932) Flagellates of the genus Trichonympha in termites. Univ Calif (Berkeley) Publ Zool 37 : 349 476.
22. Kitade, O., Maeyama, T. Matsumoto, T. (1997) Establishment of symbiotic flagellate fauna of Hodotermopsis japonica (Isoptera: Termopsidae). Sociobiology 30 : 161 167.
23. Klein, M., Friedrich, M., Roger, A.J., Hugenholtz, P., Fishbain, S., Abicht, H., et al. (2001) Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J Bacteriol 183 : 6028 6035.
24. Kuhnigk, T., Branke, J., Krekeler, D., Cypionka, H. König, H. (1996) A feasible role of sulfer-reducing bacteria in the termite gut. Syst Appl Microbiol 19 : 139 149.
25. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, et al. (2004) ARB: a software environment for sequence data. Nucl Acids Res 32 : 1363 1371.
26. Maidak, B.L., Cole, J.R., Lilburn, T.G., Parker, C.T.J., Saxman, P.R., Farris, R.J., et al. (2001) The RDP-II (Ribosomal Database Project). Nucleic Acids Res 29 : 173 174.
27. Muyzer, G. Stams, A.J. (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6 : 441 454.
28. Noda, S., Inoue, T., Hongoh, Y., Kawai, M., Nalepa, C.A., Vongkaluang, C., et al. (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.
29. Ohkuma, M. (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16 : 345 352.
30. Ohkuma, M., Ohtoko, K., Iida, T., Tokura, M., Moriya, S., Usami, R., et al. (2000) Phylogenetic identification of hypermastigotes, Pseudotrichonympha, Spirotrichonympha, Holomastigotoides, and parabasalian symbionts in the hindgut of termites. J Euk Microbiol 47 : 249 259.
31. 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.
32. Postgate, J.R. (1979) The Sulphate-Reducing Bacteria. Cambridge, UK : Cambridge University Press.
33. Romao, C.V., Pereira, I.A., Xavier, A.V., LeGall, J. Teixeira, M. (1997) Characterization of the [NiFe] hydrogenase from the sulfate reducer Desulfovibrio vulgaris Hildenborough. Biochem Biophys Res Commun 240 : 75 79.
34. Schramm, A., Fuchs, B.M., Nielsen, J.L., Tonolla, M. Stahl, D.A. (2002) Fluorescence in situ hybridization of 16S rRNA gene clones (Clone-FISH) for probe validation and screening of clone libraries. Environ Microbiol 4 : 713 720.
35. 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.
36. Thongaram, T., Kosono, S., Ohkuma, M., Hongoh, Y., Kitada, M., Yoshinaka, T., et al. (2003) Gut of higher termites as a niche for alkaliphiles as shown by culture-based and culture-independent studies. Microbes Environ 18 : 152 159.
37. Vu, A.T., Nguyen, N.C. Leadbetter, J.R. (2004) Iron reduction in the metal-rich guts of wood-feeding termites. Geobiology 2 : 239 247.
38. Widdel, F. (1988) Microbiology and ecology of sulfate- and sulfur-reducing bacteria. In Biology of Anaerobic Microorganisms. Zehnder, A.J.B. (ed.). New York, USA : John Wiley & Sons, pp. 469 586.
39. Widdel, F. Hansen, T.A. (1992) The dissimilatory sulfate- and sulfur-reducing bacteria. In The Prokaryotes (2nd ed.). Balows, A., Trüper, H.G., Dworkin, M., Harder, W. Schleifer, K.-H. (eds). New York, USA : Springer-Verlag, pp. 583 624.
40. Yamin, M.A. (1981) Cellulose metabolism by the flagellate Trichonympha from a termite is independent of endosymbiotic bacteria. Science 211 : 58 59.
41. Zverlov, V., Klein, M., Lucker, S., Friedrich, M.W., Kellermann, J., Stahl, D.A., et al. (2005) Lateral gene transfer of dissimilatory (bi)sulfite reductase revisited. J Bacteriol 187 : 2203 2208.