Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut

Cellular and Molecular Life Sciences

Volumn 68, Issue 8, 2011, Pages 1311-1325

  Hongoh, Yuichi ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Gut bacteria; Insect; Lignocellulose; Nitrogen fixation; Whole genome amplification

Indexed keywords

BETA GLUCOSIDASE; CELLULASE; GLYCOSIDASE; HEMICELLULOSE; HYDROGEN; LACCASE; LIGNOCELLULOSE;

ARCHAEBACTERIUM; ENDOSYMBIOSIS; ENZYME ACTIVITY; EXPRESSED SEQUENCE TAG; FERMENTATION; GENE EXPRESSION; GENOME ANALYSIS; GLYCOLYSIS; HYDROLYSIS; INTESTINE FLORA; ISOPTERA; METAGENOMICS; NITROGEN FIXATION; NITROGEN METABOLISM; NONHUMAN; PHYLOGENY; PROTEOMICS; REVIEW; SYMBIOSIS; WOOD;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; EVOLUTION, MOLECULAR; GASTROINTESTINAL TRACT; ISOPTERA; LIGNIN; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EUKARYOTA; HEXAPODA; ISOPTERA; PROTISTA;

EID: 79953688970     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0648-z     Document Type: Review

References (123)

1. DJ Inward AP Vogler P Eggleton 2007 A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology Mol Phylogenet Evol 44 953 967 17625919 1:CAS:528:DC%2BD2sXpt1als7g%3D (Pubitemid 47259721)
2. N Lo MS Engel S Cameron CA Nalepa G Tokuda D Grimaldi O Kitade K Krishna KD Klass K Maekawa T Miura GJ Thompson 2007 Save Isoptera: a comment on Inward et al Biol Lett 3 562 565 17698448
3. Sugimoto A, Bignell DE, Macdonald J (2000) Global impact of termites on the carbon cycle. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht
4. Vinson SB (ed) (1986) Economic impact and control of social insects. Praeger, New York
5. Kambhampati S, Eggleton P (2000) Taxonomy and phylogeny of termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiose, ecology. Kluwer Academic Publishers, Dordrecht
6. M Ohkuma H Yuzawa W Amornsak Y Sornnuwat Y Takematsu A Yamada C Vongkaluang O Sarnthoy N Kirtibutr N Noparatnaraporn T Kudo T Inoue 2004 Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences Mol Phylogenet Evol 31 701 710 15062804 1:CAS:528:DC%2BD2cXivVKntbc%3D (Pubitemid 38504458)
7. H Watanabe G Tokuda 2001 Animal cellulases Cell Mol Life Sci 58 1167 1178 11577976 1:CAS:528:DC%2BD3MXnt12gsLc%3D (Pubitemid 32844091)
8. H Watanabe G Tokuda 2010 Cellulolytic systems in insects Annu Rev Entomol 55 609 632 19754245 1:CAS:528:DC%2BC3cXptVSgtA%3D%3D
9. Y Hongoh 2010 Diversity and genomes of uncultured microbial symbionts in the termite gut Biosci Biotechnol Biochem 74 1145 1151 20530908 1:CAS:528:DC%2BC3cXovFeju7s%3D
10. C Noirot 1995 The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. I. Lower termites Ann Soc Entomol Fr (NS) 31 197 226
11. C Noirot 2001 The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. II. Higher termites (Termitidae) Ann Soc Entomol Fr (NS) 37 431 471 (Pubitemid 33588865)
12. A Fujita M Hojo T Aoyagi Y Hayashi G Arakawa G Tokuda H Watanabe 2010 Details of the digestive system in the midgut of Coptotermes formosanus Shiraki J Wood Sci 56 222 226 1:CAS:528:DC%2BC3cXnvVyjur0%3D
13. G Tokuda N Lo H Watanabe M Slaytor T Matsumoto H Noda 1999 Metazoan cellulase genes from termites: intron/exon structures and sites of expression Biochim Biophys Acta 1447 146 159 10542312 1:CAS:528:DyaK1MXntVGksL4%3D (Pubitemid 29494987)
14. K Nakashima H Watanabe H Saitoh G Tokuda JI Azuma 2002 Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki Insect Biochem Mol Biol 32 777 784 12044494 1:CAS:528: DC%2BD38XktVGjsL0%3D (Pubitemid 34601759)
15. G Tokuda H Saito H Watanabe 2002 A digestive beta-glucosidase from the salivary glands of the termite, Neotermes koshunensis (Shiraki): distribution, characterization and isolation of its precursor cDNA by 5′- and 3′-RACE amplifications with degenerate primers Insect Biochem Mol Biol 32 1681 1689 12429120 1:CAS:528:DC%2BD38XosFChsro%3D (Pubitemid 35368817)
16. G Tokuda N Lo H Watanabe G Arakawa T Matsumoto H Noda 2004 Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage Mol Ecol 13 3219 3228 15367134 1:CAS:528: DC%2BD2cXptFSrsbo%3D (Pubitemid 39301080)
17. G Tokuda M Miyagi H Makiya H Watanabe G Arakawa 2009 Digestive beta-glucosidases from the wood-feeding higher termite, Nasutitermes takasagoensis: intestinal distribution, molecular characterization, and alteration in sites of expression Insect Biochem Mol Biol 39 931 937 19944757 1:CAS:528:DC%2BC3cXktVaquw%3D%3D
18. M Yuki S Moriya T Inoue T Kudo 2008 Transcriptome analysis of the digestive organs of Hodotermopsis sjoestedti, a lower termite that hosts mutualistic microorganisms in its hindgut Zool Sci 25 401 406 18459822 1:CAS:528:DC%2BD1cXhtF2itLbK (Pubitemid 351852347)
19. A Tartar MM Wheeler X Zhou MR Coy DG Boucias ME Scharf 2009 Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes Biotechnol Biofuels 2 e25
20. Bignell DE (2000) Introduction to symbiosis. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht
21. Breznak JA (2000) Ecology of prokaryotic microbes in the guts of wood- and litter-feeding termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht
22. BL Cantarel PM Coutinho C Rancurel T Bernard V Lombard B Henrissat 2009 The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Nucl Acids Res 37 D233 D238 18838391 1:CAS:528:DC%2BD1cXhsFejtL7K
23. A Davison M Blaxter 2005 Ancient origin of glycosyl hydrolase family 9 cellulase genes Mol Biol Evol 22 1273 1284 15703240 1:CAS:528: DC%2BD2MXjvVKitbc%3D (Pubitemid 40577765)
24. N Lo H Watanabe M Sugimura 2003 Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals Proc R Soc Lond B 270 Suppl 1 S69 S72 1:CAS:528:DC%2BD3sXns1Smsb0%3D
25. C Eggert U Temp JF Dean KE Eriksson 1996 A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase FEBS Lett 391 144 148 8706903 1:CAS:528:DyaK28XkvFWitLw%3D (Pubitemid 26325732)
26. Y Arakane S Muthukrishnan RW Beeman MR Kanost KJ Kramer 2005 Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning Proc Natl Acad Sci USA 102 11337 11342 16076951 1:CAS:528:DC%2BD2MXoslKitL4%3D (Pubitemid 41153821)
27. MR Coy TZ Salem JS Denton ES Kovaleva Z Liu DS Barber JH Campbell DC Davis GW Buchman DG Boucias ME Scharf 2010 Phenol-oxidizing laccases from the termite gut Insect Biochem Mol Biol 40 723 732 20691784 1:CAS:528: DC%2BC3cXht1WhtL3I
28. JA Breznak A Brune 1994 Role of microorganisms in the digestion of lignocellulose by termites Annu Rev Entomol 39 453 487 1:CAS:528: DyaK2cXhsF2itbo%3D
29. M Ohkuma 2003 Termite symbiotic systems: efficient bio-recycling of lignocellulose Appl Microbiol Biotechnol 61 1 9 12658509 1:CAS:528: DC%2BD3sXitlKhtrw%3D (Pubitemid 36458047)
30. SM Geib TR Filley PG Hatcher K Hoover JE Carlson MD Jimenez-Gasco A Nakagawa-Izumi RL Sleighter M Tien 2008 Lignin degradation in wood-feeding insects Proc Natl Acad Sci USA 105 12932 12937 18725643 1:CAS:528: DC%2BD1cXhtFSjsbvP
31. T Johjima T Inoue M Ohkuma N Noparatnaraporn T Kudo 2003 Chemical analysis of food processing by the fungus-growing termite Macrotermes gilvus Sociobiology 42 815 824 (Pubitemid 37457771)
32. Y Taprab T Johjima Y Maeda S Moriya S Trakulnaleamsai N Noparatnaraporn M Ohkuma T Kudo 2005 Symbiotic fungi produce laccases potentially involved in phenol degradation in fungus combs of fungus-growing termites in Thailand Appl Environ Microbiol 71 7696 7704 16332742 1:CAS:528:DC%2BD2MXhtlehtL3F (Pubitemid 41803888)
33. F Warnecke P Luginbühl N Ivanova M Ghassemian TH Richardson JT Stege M Cayouette AC McHardy G Djordjevic N Aboushadi R Sorek SG Tringe M Podar HG Martin V Kunin D Dalevi J Madejska E Kirton D Platt E Szeto A Salamov K Barry N Mikhailova NC Kyrpides EG Matson EA Ottesen X Zhang M Hernandez C Murillo LG Acosta I Rigoutsos G Tamayo BD Green C Chang EM Rubin EJ Mathur DE Robertson P Hugenholtz JR Leadbetter 2007 Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite Nature 450 560 565 18033299 1:CAS:528:DC%2BD2sXhtlCrtb3J (Pubitemid 350190243)
34. RE Hungate 1938 Studies on the nutrition of Zootermopsis II. The relative importance of termite and the protozoa in wood digestion Ecology 19 1 25
35. T Inoue K Murashima J-I Azuma A Sugimoto M Slaytor 1997 Cellulose and xylan utilisation in the lower termite Reticulitermes speratus J Insect Physiol 43 235 242 12769907 1:CAS:528:DyaK2sXitVGktrw%3D (Pubitemid 27324700)
36. G Tokuda N Lo E Watanabe 2005 Marked variations in patterns of cellulase activity against crystalline- vs. carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites Physiol Entomol 30 372 380 1:CAS:528:DC%2BD28XntlSksw%3D%3D (Pubitemid 41784903)
37. MA Yamin 1979 Flagellates of the orders Trichomonadida Kirby, Oxymonadida Grassé, and Hypermastigida Grassi and 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
38. O Kitade T Matsumoto 1998 Characteristics of the symbiotic flagellate composition within the termite family Rhinotermitidae (Isoptera) Symbiosis 25 271 278 (Pubitemid 28385891)
39. T Yoshimura 1995 Contribution of the protozoan fauna to nutritional physiology of the lower termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) Wood Res 82 68 129
40. LI Katzin H Kirby 1939 The relative weights of termites and their protozoa J Parasitol 25 444 445
41. LR Cleveland 1923 Symbiosis between termites and their intestinal protozoa Proc Natl Acad Sci USA 9 424 428 16586922 1:STN:280: DC%2BD28zhsFyhtw%3D%3D
42. LR Cleveland 1924 The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes Kollar Biol Bull 46 178 227
43. W Trager 1934 The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa Biol Bull 66 182 190
44. MA Yamin 1978 Axenic cultivation of the cellulolytic flagellate Trichomitopsis termopsidis (Cleveland) from the termite Zootermopsis J Protozool 25 535 538
45. MA Yamin 1981 Cellulose metabolism by the flagellate Trichonympha from a termite is independent of endosymbiotic bacteria Science 211 58 59 17731245 1:CAS:528:DyaL3MXmtFertg%3D%3D
46. MA Yamin 1980 Cellulose metabolism by the termite flagellate Trichomitopsis termopsidis Appl Environ Microbiol 39 859 863 16345549 1:CAS:528:DyaL3cXktVeltLc%3D (Pubitemid 10038178)
47. RE Hungate 1939 Experiments on the nutrition of Zootermopsis. III. The anaerobic carbohydrate dissimilation by the intestinal protozoa Ecology 20 230 245 1:CAS:528:DyaH3cXksFyjug%3D%3D
48. RE Hungate 1943 Quantitative analyses of the cellulose fermentation by termite protozoa Ann Entomol Soc Am 36 730 739 1:CAS:528:DyaH2cXltlWh
49. DA Odelson JA Breznak 1983 Volatile fatty acid production by the hindgut microbiota of xylophagous termites Appl Environ Microbiol 45 1602 1613 16346296 1:CAS:528:DyaL3sXktVartbs%3D (Pubitemid 13055044)
50. A Brune D Emerson JA Breznak 1995 The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites Appl Environ Microbiol 61 2681 2687 16535076 1:CAS:528:DyaK2MXms1Grsrg%3D
51. DA Odelson JA Breznak 1985 Nutrition and growth characteristics of Trichomitopsis termopsidis, a cellulolytic protozoan from termites Appl Environ Microbiol 49 614 621 16346754 1:CAS:528:DyaL2MXhvVais7g%3D (Pubitemid 15138050)
52. DA Odelson JA Breznak 1985 Cellulase and other polymer-hydrolyzing activities of Trichomitopsis termopsidis, a symbiotic protozoan from termites Appl Environ Microbiol 49 622 626 16346755 1:CAS:528:DyaL2MXhsVGrs78%3D (Pubitemid 15138051)
53. K Ohtoko M Ohkuma S Moriya T Inoue R Usami T Kudo 2000 Diverse genes of cellulase homologues of glycosyl hydrolase family 45 from the symbiotic protists in the hindgut of the termite Reticulitermes speratus Extremophiles 4 343 349 11139076 1:CAS:528:DC%2BD3MXlt1Gjsg%3D%3D
54. L Li J Fröhlich P Pfeiffer H König 2003 Termite gut symbiotic archaezoa are becoming living metabolic fossils Eukaryot Cell 2 1091 1098 14555492 1:CAS:528:DC%2BD3sXos1Gkurk%3D (Pubitemid 37298723)
55. H Watanabe K Nakashima H Saito M Slaytor 2002 New endo-beta-1, 4-glucanases from the parabasalian symbionts, Pseudotrichonympha grassii and Holomastigotoides mirabile of Coptotermes termites Cell Mol Life Sci 59 1983 1992 12530528 1:CAS:528:DC%2BD38Xps1enuro%3D (Pubitemid 36015870)
56. T Inoue S Moriya M Ohkuma T Kudo 2005 Molecular cloning and characterization of a cellulase gene from a symbiotic protist of the lower termite, Coptotermes formosanus Gene 349 67 75 15777663 1:CAS:528: DC%2BD2MXjtFOls7c%3D
57. KI Nakashima H Watanabe JI Azuma 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 12440775 1:CAS:528:DC%2BD38Xotlahu74%3D (Pubitemid 35239309)
58. N Todaka S Moriya K Saita T Hondo I Kiuchi H Takasu M Ohkuma C Piero Y Hayashizaki T Kudo 2007 Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus FEMS Microbiol Ecol 59 592 599 17239084 1:CAS:528:DC%2BD2sXjsVyqu78%3D (Pubitemid 46376236)
59. O Kitade T Matsumoto 1993 Symbiotic protistan faunae of Reticulitermes (Isoptera: Rhinotermitidae) in the Japan Archipelago Sociobiology 23 135 153
60. N Todaka T Inoue K Saita M Ohkuma CA Nalepa M Lenz T Kudo S Moriya 2010 Phylogenetic analysis of cellulolytic enzyme genes from representative lineages of termites and a related cockroach PLoS One 5 e8636 20072608
61. M Wenzel M Shönig M Berchtold P Kämpfer H König 2002 Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis J Appl Microbiol 92 32 40 11849325 1:STN:280:DC%2BD387jsF2rtw%3D%3D (Pubitemid 34205944)
62. A Brune M Kuhl 1996 pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes J Insect Physiol 42 1121 1127 1:CAS:528:DyaK2sXot1Oitw%3D%3D (Pubitemid 27521832)
63. DE Bignell P Eggleton 1995 On the elevated intestinal pH of higher termites (Isoptera: Termitidae) Insect Soc 42 57 69
64. RT Czolij M Slaytor RW O'Brien 1985 Bacterial flora of the mixed segment and the hindgut of the higher termite Nasutitermes exitiosus Hill (Termitidae, Nasutitermitinae) Appl Environ Microbiol 49 1226 1236
65. G Tokuda I Yamaoka H Noda 2000 Localization of symbiotic clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki) Appl Environ Microbiol 66 2199 2207 10788400 1:CAS:528:DC%2BD3cXjtV2ksr0%3D (Pubitemid 30253751)
66. M Slaytor 1992 Cellulose digestion in termites and cockroaches: what role do symbionts play? Comp Biochem Physiol B Biochem Mol Biol 103 775 784
67. G Tokuda H Watanabe 2007 Hidden cellulases in termites: revision of an old hypothesis Biol Lett 3 336 339 17374589 1:CAS:528:DC%2BD2sXnt1Gksr8%3D
68. TG Lilburn TM Schmidt JA Breznak 1999 Phylogenetic diversity of termite gut spirochaetes Environ Microbiol 1 331 345 11207751 1:CAS:528: DyaK1MXmtFOrtbc%3D
69. Y Hongoh P Deevong T Inoue S Moriya S Trakulnaleamsai M Ohkuma C Vongkaluang N Noparatnaraporn T Kudo 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 16269686 1:CAS:528:DC%2BD2MXht1ektbbP (Pubitemid 43194141)
70. BJ Paster FE Dewhirst SM Cooke V Fussing LK Poulsen JA Breznak 1996 Phylogeny of not-yet-cultured spirochetes from termite guts Appl Environ Microbiol 62 347 352 8593040 1:CAS:528:DyaK28XovVCntA%3D%3D (Pubitemid 26047402)
71. Y Hongoh M Ohkuma T Kudo 2003 Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae) FEMS Microbiol Ecol 44 231 242 19719640 1:CAS:528:DC%2BD3sXjtFWrsrk%3D (Pubitemid 36423418)
72. Y Hongoh P Deevong S Hattori T Inoue S Noda N Noparatnaraporn T Kudo M Ohkuma 2006 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 17021231 1:CAS:528:DC%2BD28XhtFalsLnP (Pubitemid 44582922)
73. Burnum KE, Callister SJ, Nicora CD, Purvine SO, Hugenholtz P, Warnecke F, Scheffrahn RH, Smith RD, Lipton MS (2011) Proteome insights into the symbiotic relationship between a captive colony of Nasutitermes corniger and its hindgut microbiome. ISME J 5:161-164
74. M Pester A Brune 2007 Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts ISME J 1 551 565 18043656 1:CAS:528:DC%2BD2sXht1yktLrI (Pubitemid 47530660)
75. A Ebert A Brune 1997 Hydrogen concentration profiles at the oxic-anoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar) Appl Environ Microbiol 63 4039 4046 16535716 1:CAS:528:DyaK2sXms1Sgt70%3D (Pubitemid 27411368)
76. J Inoue K Saita T Kudo S Ui M Ohkuma 2007 Hydrogen production by termite gut protists: characterization of iron hydrogenases of parabasalian symbionts of the termite Coptotermes formosanus Eukaryot Cell 6 1925 1932 17766465 1:CAS:528:DC%2BD2sXht1Smu7vI (Pubitemid 47585580)
77. JR Graber JR Leadbetter JA Breznak 2004 Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts Appl Environ Microbiol 70 1315 1320 15006748 1:CAS:528:DC%2BD2cXisVKjtb0%3D (Pubitemid 38365108)
78. 2 by termite gut microbes Appl Environ Microbiol 52 623 630 16347157 1:CAS:528:DyaL28XmtVGqsLc%3D (Pubitemid 16004634)
79. 2-utilizing acetogen isolated from termites Arch Microbiol 150 282 288 1:CAS:528:DyaL1cXltVOntbg%3D
80. 2 acetogenic bacterium from the termite, Pterotermes occidentis Arch Microbiol 156 91 98 1723588 1:CAS:528:DyaK3MXmtVartLg%3D
81. 2 by spirochetes from termite guts Science 283 686 689 9924028 1:CAS:528:DyaK1MXot1yhtw%3D%3D
82. 2-acetogenic spirochete from termite hindguts Appl Environ Microbiol 70 1307 1314 15006747 1:CAS:528:DC%2BD2cXisVKjtbw%3D (Pubitemid 38365107)
83. TM Salmassi JR Leadbetter 2003 Analysis of genes of tetrahydrofolate- dependent metabolism from cultivated spirochaetes and the gut community of the termite Zootermopsis angusticollis Microbiology 149 2529 2537 12949177 1:CAS:528:DC%2BD3sXnslGnsLg%3D (Pubitemid 37160727)
84. EA Ottesen JW Hong SR Quake JR Leadbetter 2006 Microfluidic digital PCR enables multigene analysis of individual environmental bacteria Science 314 1464 1467 17138901 1:CAS:528:DC%2BD28Xht1CntrnM (Pubitemid 44871954)
85. M Pester A Brune 2006 Expression profiles of fhs (FTHFS) genes support the hypothesis that spirochaetes dominate reductive acetogenesis in the hindgut of lower termites Environ Microbiol 8 1261 1270 16817934 1:CAS:528: DC%2BD28XnsVCksb4%3D (Pubitemid 43901756)
86. MJ Lee PJ Schreurs AC Messer SH Zinder 1987 Association of methanogenic bacteria with flagellated protozoa from a termite gut Curr Microbiol 15 337 341
87. J Inoue S Noda Y Hongoh S Ui M Ohkuma 2008 Identification of endosymbiotic methanogen and ectosymbiotic spirochetes of gut protists of the termite Coptotermes formosanus Microbes Environ 23 94 97
88. M Tokura M Ohkuma T Kudo 2000 Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites FEMS Microbiol Ecol 33 233 240 11098074 1:CAS:528:DC%2BD3cXmvFyrurk%3D
89. A Brauman J Dore P Eggleton DE Bignell JA Breznak MD Kane 2001 Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits FEMS Microbiol Ecol 35 27 36 11248387 1:CAS:528:DC%2BD3MXhvVagsrk%3D (Pubitemid 32436359)
90. SE Donovan KJ Purdy MD Kane P Eggleton 2004 Comparison of Euryarchaea strains in the guts and food-soil of the soil-feeding termite Cubitermes fungifaber across different soil types Appl Environ Microbiol 70 3884 3892 15240259 1:CAS:528:DC%2BD2cXmtFWnsbo%3D (Pubitemid 38969725)
91. JR Leadbetter JA Breznak 1996 Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes Appl Environ Microbiol 62 3620 3631 8837417 1:CAS:528:DyaK28XmtVGlt70%3D (Pubitemid 26329586)
92. JR Leadbetter LD Crosby JA Breznak 1998 Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts Arch Microbiol 169 287 292 9531629 1:CAS:528:DyaK1cXivVWgtb4%3D (Pubitemid 28189532)
93. KJ Purdy 2007 The distribution and diversity of Euryarchaeota in termite guts Adv Appl Microbiol 62 63 80 17869602 1:CAS:528:DC%2BD1cXht1Wks7o%3D (Pubitemid 47380496)
94. Hongoh Y, Ohkuma M (2011) Termite gut flagellates and their methanogenic and eubacterial symbionts. In: Hackstein JHP (ed) Microbiology monographs 19: (Endo)symbiotic Methanogenic Archaea. Springer, Berlin
95. Brune A (2011) Methanogens in the digestive tract of termites. In: Hackstein JHP (ed) Microbiology monographs 19: (Endo)symbiotic Methanogenic Archaea. Springer, Berlin
96. JA Breznak WJ Brill JW Mertins HC Coppel 1973 Nitrogen fixation in termites Nature 244 577 580 4582514 1:CAS:528:DyaE2cXht1Oguw%3D%3D
97. JR Benemann 1973 Nitrogen fixation in termites Science 181 164 165 17746626 1:CAS:528:DyaE3sXks1eltLw%3D
98. M Ohkuma S Noda T Kudo 1999 Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites Appl Environ Microbiol 65 4926 4934 10543805 1:CAS:528:DyaK1MXnt1Wmtbk%3D
99. S Noda M Ohkuma R Usami K Horikoshi T Kudo 1999 Culture-independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis Appl Environ Microbiol 65 4935 4942 10543806 1:CAS:528:DyaK1MXnt1WmtbY%3D
100. S Noda M Ohkuma T Kudo 2002 Nitrogen fixation genes expressed in symbiotic microbial community in the gut of the termite Coptotermes formosanus Microbes Environ 17 139 143
101. TG Lilburn KS Kim NE Ostrom KR Byzek JR Leadbetter JA Breznak 2001 Nitrogen fixation by symbiotic and free-living spirochetes Science 292 2495 2498 11431569 1:CAS:528:DC%2BD3MXkvFWls74%3D (Pubitemid 32601662)
102. U Stingl A Maass R Radek A Brune 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 15256565 1:CAS:528:DC%2BD2cXmtFGrtb0%3D (Pubitemid 39117635)
103. S Noda T Inoue Y Hongoh M Kawai CA Nalepa C Vongkaluang T Kudo M Ohkuma 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 16343317 1:CAS:528: DC%2BD28XitFSgtbo%3D
104. S Noda Y Hongoh T Sato M Ohkuma 2009 Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites BMC Evol Biol 9 e158
105. MS Desai JFH Strassert K Meuser H Hertel W Ikeda-Ohtsubo R Radek A Brune 2010 Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae) Environ Microbiol 12 2120 2132 1:CAS:528:DC%2BC3cXhtFegsLbO
106. Y Hongoh T Sato MF Dolan S Noda S Ui T Kudo M Ohkuma 2007 The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the "Synergistes" group Appl Environ Microbiol 73 6270 6276 17675420 1:CAS:528:DC%2BD2sXhtFGmtrjP (Pubitemid 47548038)
107. Y Hongoh T Sato S Noda S Ui T Kudo M Ohkuma 2007 Candidatus Symbiothrix dinenymphae: bristle-like Bacteroidales ectosymbionts of termite gut protists Environ Microbiol 9 2631 2635 17803785 1:CAS:528:DC%2BD2sXht1GqsLzI (Pubitemid 47366659)
108. LR Cleveland AV Grimstone 1964 The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms Proc R Soc Lond B 159 668 686
109. T Iida M Ohkuma K Ohtoko T Kudo 2000 Symbiotic spirochetes in the termite hindgut: phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists FEMS Microbiol Ecol 34 17 26 11053732 1:CAS:528:DC%2BD3cXosVyrt7Y%3D
110. S Noda M Ohkuma A Yamada Y Hongoh T Kudo 2003 Phylogenetic position and in situ identification of ectosymbiotic spirochetes on protists in the termite gut Appl Environ Microbiol 69 625 633 12514050 1:CAS:528:DC%2BD3sXkvVejsg%3D%3D (Pubitemid 36077530)
111. S Noda T Iida O Kitade H Nakajima T Kudo M Ohkuma 2005 Endosymbiotic Bacteroidales bacteria of the flagellated protist Pseudotrichonympha grassii in the gut of the termite Coptotermes formosanus Appl Environ Microbiol 71 8811 8817 16332877 1:CAS:528:DC%2BD2MXhtlehtbbN (Pubitemid 41804018)
112. S Noda O Kitade T Inoue M Kawai M Kanuka K Hiroshima Y Hongoh R Constantino V Uys J-H Zhong T Kudo M Ohkuma 2007 Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts Mol Ecol 16 1257 1266 17391411 1:CAS:528:DC%2BD2sXkvVKrur8%3D (Pubitemid 46357396)
113. U Stingl R Radek H Yang A Brune 2005 "Endomicrobia": cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes Appl Environ Microbiol 71 1473 1479 15746350 1:CAS:528: DC%2BD2MXisVOisLY%3D (Pubitemid 40396686)
114. M Ohkuma T Sato S Noda S Ui T Kudo Y Hongoh 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 17391329 1:CAS:528:DC%2BD2sXmsFemurk%3D (Pubitemid 46802121)
115. W Ikeda-Ohtsubo M Desai U Stingl A Brune 2007 Phylogenetic diversity of 'Endomicrobia' and their specific affiliation with termite gut flagellates Microbiology 153 3458 3465 17906144 1:CAS:528:DC%2BD2sXht1SmurjN (Pubitemid 47629550)
116. W Ikeda-Ohtsubo A Brune 2009 Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and 'Candidatus Endomicrobium trichonymphae' Mol Ecol 18 332 342 19192183 1:CAS:528: DC%2BD1MXivVGktbc%3D
117. M Ohkuma T Kudo 1996 Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus Appl Environ Microbiol 62 461 468 8593049 1:CAS:528:DyaK28XovVCltg%3D%3D (Pubitemid 26051567)
118. J Fröhlich H König 1999 Rapid isolation of single microbial cells from mixed natural and laboratory populations with the aid of a micromanipulator Syst Appl Microbiol 22 249 257 10390876 (Pubitemid 29267505)
119. T Sato Y Hongoh S Noda S Hattori S Ui M Ohkuma 2009 Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut Environ Microbiol 11 1007 1015 19170725
120. A Brune U Stingl 2006 Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis Prog Mol Subcell Biol 41 39 60 16623388 1:CAS:528:DC%2BD28XjtlCnsLg%3D
121. M Ohkuma 2008 Symbioses of flagellates and prokaryotes in the gut of lower termites Trends Microbiol 16 345 352 18513972 1:CAS:528: DC%2BD1cXotlajsb4%3D
122. Y Hongoh VK Sharma T Prakash S Noda TD Taylor T Kudo Y Sakaki A Toyoda M Hattori M Ohkuma 2008 Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell Proc Natl Acad Sci USA 105 5555 5560 18391199 1:CAS:528:DC%2BD1cXkslSntrk%3D (Pubitemid 351753901)
123. 2 fixation to cellulolysis within protist cells in termite gut Science 322 1108 1109 19008447 1:CAS:528:DC%2BD1cXhtlGgsr7O