Cellular and Molecular Life Sciences

, Volume 68, Issue 8, pp 1311–1325 | Cite as

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

  • Yuichi Hongoh
Multi-author review


Termites thrive on dead plant matters with the aid of microorganisms resident in their gut. The gut microbiota comprises protists (single-celled eukaryotes), bacteria, and archaea, most of which are unique to the termite gut ecosystem. Although this symbiosis has long been intriguing researchers of both basic and applied sciences, its detailed mechanism remains unclear due to the enormous complexity and the unculturability of the microbiota. In the effort to overcome the difficulty, recent advances in omics, such as metagenomics, metatranscriptomics, and metaproteomics have gradually unveiled the black box of this symbiotic system. Genomics targeting a single species of the unculturable microbial members has also provided a great progress in the understanding of the symbiotic interrelationships among the gut microorganisms. In this review, the symbiotic system organized by wood-feeding termites and their gut microorganisms is outlined, focusing on the recent achievement in omics studies of this multilayered symbiotic system.


Gut bacteria Insect Lignocellulose Nitrogen fixation Whole genome amplification 


  1. 1.
    Inward DJ, Vogler AP, Eggleton P (2007) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phylogenet Evol 44:953–967PubMedGoogle Scholar
  2. 2.
    Lo N, Engel MS, Cameron S, Nalepa CA, Tokuda G, Grimaldi D, Kitade O, Krishna K, Klass KD, Maekawa K, Miura T, Thompson GJ (2007) Save Isoptera: a comment on Inward et al. Biol Lett 3:562–565PubMedGoogle Scholar
  3. 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, DordrechtGoogle Scholar
  4. 4.
    Vinson SB (ed) (1986) Economic impact and control of social insects. Praeger, New YorkGoogle Scholar
  5. 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, DordrechtGoogle Scholar
  6. 6.
    Ohkuma M, Yuzawa H, Amornsak W, Sornnuwat Y, Takematsu Y, Yamada A, Vongkaluang C, Sarnthoy O, Kirtibutr N, Noparatnaraporn N, Kudo T, Inoue T (2004) Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences. Mol Phylogenet Evol 31:701–710PubMedGoogle Scholar
  7. 7.
    Watanabe H, Tokuda G (2001) Animal cellulases. Cell Mol Life Sci 58:1167–1178PubMedGoogle Scholar
  8. 8.
    Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632PubMedGoogle Scholar
  9. 9.
    Hongoh Y (2010) Diversity and genomes of uncultured microbial symbionts in the termite gut. Biosci Biotechnol Biochem 74:1145–1151PubMedGoogle Scholar
  10. 10.
    Noirot C (1995) The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. I. Lower termites. Ann Soc Entomol Fr (NS) 31:197–226Google Scholar
  11. 11.
    Noirot C (2001) The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. II. Higher termites (Termitidae). Ann Soc Entomol Fr (NS) 37:431–471Google Scholar
  12. 12.
    Fujita A, Hojo M, Aoyagi T, Hayashi Y, Arakawa G, Tokuda G, Watanabe H (2010) Details of the digestive system in the midgut of Coptotermes formosanus Shiraki. J Wood Sci 56:222–226Google Scholar
  13. 13.
    Tokuda G, Lo N, Watanabe H, Slaytor M, Matsumoto T, Noda H (1999) Metazoan cellulase genes from termites: intron/exon structures and sites of expression. Biochim Biophys Acta 1447:146–159PubMedGoogle Scholar
  14. 14.
    Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI (2002) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32:777–784PubMedGoogle Scholar
  15. 15.
    Tokuda G, Saito H, Watanabe H (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 32:1681–1689PubMedGoogle Scholar
  16. 16.
    Tokuda G, Lo N, Watanabe H, Arakawa G, Matsumoto T, Noda H (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol Ecol 13:3219–3228PubMedGoogle Scholar
  17. 17.
    Tokuda G, Miyagi M, Makiya H, Watanabe H, Arakawa G (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 39:931–937PubMedGoogle Scholar
  18. 18.
    Yuki M, Moriya S, Inoue T, Kudo T (2008) Transcriptome analysis of the digestive organs of Hodotermopsis sjoestedti, a lower termite that hosts mutualistic microorganisms in its hindgut. Zool Sci 25:401–406PubMedGoogle Scholar
  19. 19.
    Tartar A, Wheeler MM, Zhou X, Coy MR, Boucias DG, Scharf ME (2009) Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnol Biofuels 2:e25Google Scholar
  20. 20.
    Bignell DE (2000) Introduction to symbiosis. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, DordrechtGoogle Scholar
  21. 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, DordrechtGoogle Scholar
  22. 22.
    Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucl Acids Res 37:D233–D238PubMedGoogle Scholar
  23. 23.
    Davison A, Blaxter M (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22:1273–1284PubMedGoogle Scholar
  24. 24.
    Lo N, Watanabe H, Sugimura M (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–S72Google Scholar
  25. 25.
    Eggert C, Temp U, Dean JF, Eriksson KE (1996) A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett 391:144–148PubMedGoogle Scholar
  26. 26.
    Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ (2005) Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Natl Acad Sci USA 102:11337–11342PubMedGoogle Scholar
  27. 27.
    Coy MR, Salem TZ, Denton JS, Kovaleva ES, Liu Z, Barber DS, Campbell JH, Davis DC, Buchman GW, Boucias DG, Scharf ME (2010) Phenol-oxidizing laccases from the termite gut. Insect Biochem Mol Biol 40:723–732PubMedGoogle Scholar
  28. 28.
    Breznak JA, Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39:453–487Google Scholar
  29. 29.
    Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61:1–9PubMedGoogle Scholar
  30. 30.
    Geib SM, Filley TR, Hatcher PG, Hoover K, Carlson JE, Jimenez-Gasco MD, Nakagawa-Izumi A, Sleighter RL, Tien M (2008) Lignin degradation in wood-feeding insects. Proc Natl Acad Sci USA 105:12932–12937PubMedGoogle Scholar
  31. 31.
    Johjima T, Inoue T, Ohkuma M, Noparatnaraporn N, Kudo T (2003) Chemical analysis of food processing by the fungus-growing termite Macrotermes gilvus. Sociobiology 42:815–824Google Scholar
  32. 32.
    Taprab Y, Johjima T, Maeda Y, Moriya S, Trakulnaleamsai S, Noparatnaraporn N, Ohkuma M, Kudo T (2005) Symbiotic fungi produce laccases potentially involved in phenol degradation in fungus combs of fungus-growing termites in Thailand. Appl Environ Microbiol 71:7696–7704PubMedGoogle Scholar
  33. 33.
    Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedGoogle Scholar
  34. 34.
    Hungate RE (1938) Studies on the nutrition of Zootermopsis II. The relative importance of termite and the protozoa in wood digestion. Ecology 19:1–25Google Scholar
  35. 35.
    Inoue T, Murashima K, Azuma J-I, Sugimoto A, Slaytor M (1997) Cellulose and xylan utilisation in the lower termite Reticulitermes speratus. J Insect Physiol 43:235–242PubMedGoogle Scholar
  36. 36.
    Tokuda G, Lo N, Watanabe E (2005) Marked variations in patterns of cellulase activity against crystalline- vs. carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol Entomol 30:372–380Google Scholar
  37. 37.
    Yamin MA (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 4:1–120Google Scholar
  38. 38.
    Kitade O, Matsumoto T (1998) Characteristics of the symbiotic flagellate composition within the termite family Rhinotermitidae (Isoptera). Symbiosis 25:271–278Google Scholar
  39. 39.
    Yoshimura T (1995) Contribution of the protozoan fauna to nutritional physiology of the lower termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Wood Res 82:68–129Google Scholar
  40. 40.
    Katzin LI, Kirby H (1939) The relative weights of termites and their protozoa. J Parasitol 25:444–445Google Scholar
  41. 41.
    Cleveland LR (1923) Symbiosis between termites and their intestinal protozoa. Proc Natl Acad Sci USA 9:424–428PubMedGoogle Scholar
  42. 42.
    Cleveland LR (1924) The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes Kollar. Biol Bull 46:178–227Google Scholar
  43. 43.
    Trager W (1934) The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol Bull 66:182–190Google Scholar
  44. 44.
    Yamin MA (1978) Axenic cultivation of the cellulolytic flagellate Trichomitopsis termopsidis (Cleveland) from the termite Zootermopsis. J Protozool 25:535–538Google Scholar
  45. 45.
    Yamin MA (1981) Cellulose metabolism by the flagellate Trichonympha from a termite is independent of endosymbiotic bacteria. Science 211:58–59PubMedGoogle Scholar
  46. 46.
    Yamin MA (1980) Cellulose metabolism by the termite flagellate Trichomitopsis termopsidis. Appl Environ Microbiol 39:859–863PubMedGoogle Scholar
  47. 47.
    Hungate RE (1939) Experiments on the nutrition of Zootermopsis. III. The anaerobic carbohydrate dissimilation by the intestinal protozoa. Ecology 20:230–245Google Scholar
  48. 48.
    Hungate RE (1943) Quantitative analyses of the cellulose fermentation by termite protozoa. Ann Entomol Soc Am 36:730–739Google Scholar
  49. 49.
    Odelson DA, Breznak JA (1983) Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol 45:1602–1613PubMedGoogle Scholar
  50. 50.
    Brune A, Emerson D, Breznak JA (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 61:2681–2687PubMedGoogle Scholar
  51. 51.
    Odelson DA, Breznak JA (1985) Nutrition and growth characteristics of Trichomitopsis termopsidis, a cellulolytic protozoan from termites. Appl Environ Microbiol 49:614–621PubMedGoogle Scholar
  52. 52.
    Odelson DA, Breznak JA (1985) Cellulase and other polymer-hydrolyzing activities of Trichomitopsis termopsidis, a symbiotic protozoan from termites. Appl Environ Microbiol 49:622–626PubMedGoogle Scholar
  53. 53.
    Ohtoko K, Ohkuma M, Moriya S, Inoue T, Usami R, Kudo T (2000) Diverse genes of cellulase homologues of glycosyl hydrolase family 45 from the symbiotic protists in the hindgut of the termite Reticulitermes speratus. Extremophiles 4:343–349PubMedGoogle Scholar
  54. 54.
    Li L, Fröhlich J, Pfeiffer P, König H (2003) Termite gut symbiotic archaezoa are becoming living metabolic fossils. Eukaryot Cell 2:1091–1098PubMedGoogle Scholar
  55. 55.
    Watanabe H, Nakashima K, Saito H, Slaytor M (2002) New endo-beta-1, 4-glucanases from the parabasalian symbionts, Pseudotrichonympha grassii and Holomastigotoides mirabile of Coptotermes termites. Cell Mol Life Sci 59:1983–1992PubMedGoogle Scholar
  56. 56.
    Inoue T, Moriya S, Ohkuma M, Kudo T (2005) Molecular cloning and characterization of a cellulase gene from a symbiotic protist of the lower termite, Coptotermes formosanus. Gene 349:67–75PubMedGoogle Scholar
  57. 57.
    Nakashima KI, Watanabe H, Azuma JI (2002) Cellulase genes from the parabasalian symbiont Pseudotrichonympha grassii in the hindgut of the wood-feeding termite Coptotermes formosanus. Cell Mol Life Sci 59:1554–1560PubMedGoogle Scholar
  58. 58.
    Todaka N, Moriya S, Saita K, Hondo T, Kiuchi I, Takasu H, Ohkuma M, Piero C, Hayashizaki Y, Kudo T (2007) Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. FEMS Microbiol Ecol 59:592–599PubMedGoogle Scholar
  59. 59.
    Kitade O, Matsumoto T (1993) Symbiotic protistan faunae of Reticulitermes (Isoptera: Rhinotermitidae) in the Japan Archipelago. Sociobiology 23:135–153Google Scholar
  60. 60.
    Todaka N, Inoue T, Saita K, Ohkuma M, Nalepa CA, 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:e8636PubMedGoogle Scholar
  61. 61.
    Wenzel M, Shönig M, Berchtold M, Kämpfer P, König H (2002) Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92:32–40PubMedGoogle Scholar
  62. 62.
    Brune A, Kuhl M (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42:1121–1127Google Scholar
  63. 63.
    Bignell DE, Eggleton P (1995) On the elevated intestinal pH of higher termites (Isoptera: Termitidae). Insect Soc 42:57–69Google Scholar
  64. 64.
    Czolij RT, Slaytor M, O’Brien RW (1985) Bacterial flora of the mixed segment and the hindgut of the higher termite Nasutitermes exitiosus Hill (Termitidae, Nasutitermitinae). Appl Environ Microbiol 49:1226–1236Google Scholar
  65. 65.
    Tokuda G, Yamaoka I, Noda H (2000) Localization of symbiotic clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki). Appl Environ Microbiol 66:2199–2207PubMedGoogle Scholar
  66. 66.
    Slaytor M (1992) Cellulose digestion in termites and cockroaches: what role do symbionts play? Comp Biochem Physiol B Biochem Mol Biol 103:775–784Google Scholar
  67. 67.
    Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339PubMedGoogle Scholar
  68. 68.
    Lilburn TG, Schmidt TM, Breznak JA (1999) Phylogenetic diversity of termite gut spirochaetes. Environ Microbiol 1:331–345PubMedGoogle Scholar
  69. 69.
    Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Vongkaluang C, Noparatnaraporn N, Kudo T (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71:6590–6599PubMedGoogle Scholar
  70. 70.
    Paster BJ, Dewhirst FE, Cooke SM, Fussing V, Poulsen LK, Breznak JA (1996) Phylogeny of not-yet-cultured spirochetes from termite guts. Appl Environ Microbiol 62:347–352PubMedGoogle Scholar
  71. 71.
    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 44:231–242PubMedGoogle Scholar
  72. 72.
    Hongoh Y, Deevong P, Hattori S, Inoue T, Noda S, Noparatnaraporn N, Kudo T, Ohkuma M (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 72:6780–6788PubMedGoogle Scholar
  73. 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 5:161–164Google Scholar
  74. 74.
    Pester M, Brune A (2007) Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J 1:551–565PubMedGoogle Scholar
  75. 75.
    Ebert A, Brune A (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 63:4039–4046PubMedGoogle Scholar
  76. 76.
    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 6:1925–1932PubMedGoogle Scholar
  77. 77.
    Graber JR, Leadbetter JR, Breznak JA (2004) Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Appl Environ Microbiol 70:1315–1320PubMedGoogle Scholar
  78. 78.
    Breznak JA, Switzer JM (1986) Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl Environ Microbiol 52:623–630PubMedGoogle Scholar
  79. 79.
    Breznak JA, Switzer JM, Seitz H-J (1988) Sporomusa termitida sp. nov., an H2/CO2-utilizing acetogen isolated from termites. Arch Microbiol 150:282–288Google Scholar
  80. 80.
    Kane MD, Breznak JA (1991) Acetonema longum gen. nov. sp. nov., an H2/CO2 acetogenic bacterium from the termite, Pterotermes occidentis. Arch Microbiol 156:91–98PubMedGoogle Scholar
  81. 81.
    Leadbetter JR, Schmidt TM, Graber JR, Breznak JA (1999) Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283:686–689PubMedGoogle Scholar
  82. 82.
    Graber JR, Breznak JA (2004) Physiology and nutrition of Treponema primitia, an H2/CO2-acetogenic spirochete from termite hindguts. Appl Environ Microbiol 70:1307–1314PubMedGoogle Scholar
  83. 83.
    Salmassi TM, Leadbetter JR (2003) Analysis of genes of tetrahydrofolate-dependent metabolism from cultivated spirochaetes and the gut community of the termite Zootermopsis angusticollis. Microbiology 149:2529–2537PubMedGoogle Scholar
  84. 84.
    Ottesen EA, Hong JW, Quake SR, Leadbetter JR (2006) Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 314:1464–1467PubMedGoogle Scholar
  85. 85.
    Pester M, Brune A (2006) Expression profiles of fhs (FTHFS) genes support the hypothesis that spirochaetes dominate reductive acetogenesis in the hindgut of lower termites. Environ Microbiol 8:1261–1270PubMedGoogle Scholar
  86. 86.
    Lee MJ, Schreurs PJ, Messer AC, Zinder SH (1987) Association of methanogenic bacteria with flagellated protozoa from a termite gut. Curr Microbiol 15:337–341Google Scholar
  87. 87.
    Inoue J, Noda S, Hongoh Y, Ui S, Ohkuma M (2008) Identification of endosymbiotic methanogen and ectosymbiotic spirochetes of gut protists of the termite Coptotermes formosanus. Microbes Environ 23:94–97PubMedGoogle Scholar
  88. 88.
    Tokura M, Ohkuma M, Kudo T (2000) Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites. FEMS Microbiol Ecol 33:233–240PubMedGoogle Scholar
  89. 89.
    Brauman A, Dore J, Eggleton P, Bignell DE, Breznak JA, Kane MD (2001) Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol Ecol 35:27–36PubMedGoogle Scholar
  90. 90.
    Donovan SE, Purdy KJ, Kane MD, Eggleton P (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 70:3884–3892PubMedGoogle Scholar
  91. 91.
    Leadbetter JR, Breznak JA (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 62:3620–3631PubMedGoogle Scholar
  92. 92.
    Leadbetter JR, Crosby LD, Breznak JA (1998) Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch Microbiol 169:287–292PubMedGoogle Scholar
  93. 93.
    Purdy KJ (2007) The distribution and diversity of Euryarchaeota in termite guts. Adv Appl Microbiol 62:63–80PubMedGoogle Scholar
  94. 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, BerlinGoogle Scholar
  95. 95.
    Brune A (2011) Methanogens in the digestive tract of termites. In: Hackstein JHP (ed) Microbiology monographs 19: (Endo)symbiotic Methanogenic Archaea. Springer, BerlinGoogle Scholar
  96. 96.
    Breznak JA, Brill WJ, Mertins JW, Coppel HC (1973) Nitrogen fixation in termites. Nature 244:577–580PubMedGoogle Scholar
  97. 97.
    Benemann JR (1973) Nitrogen fixation in termites. Science 181:164–165PubMedGoogle Scholar
  98. 98.
    Ohkuma M, Noda S, Kudo T (1999) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65:4926–4934PubMedGoogle Scholar
  99. 99.
    Noda S, Ohkuma M, Usami R, Horikoshi K, Kudo T (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 65:4935–4942PubMedGoogle Scholar
  100. 100.
    Noda S, Ohkuma M, Kudo T (2002) Nitrogen fixation genes expressed in symbiotic microbial community in the gut of the termite Coptotermes formosanus. Microbes Environ 17:139–143Google Scholar
  101. 101.
    Lilburn TG, Kim KS, Ostrom NE, Byzek KR, Leadbetter JR, Breznak JA (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498PubMedGoogle Scholar
  102. 102.
    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 150:2229–2235PubMedGoogle Scholar
  103. 103.
    Noda S, Inoue T, Hongoh Y, Kawai M, Nalepa CA, 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 8:11–20PubMedGoogle Scholar
  104. 104.
    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:e158Google Scholar
  105. 105.
    Desai MS, Strassert JFH, Meuser K, Hertel H, Ikeda-Ohtsubo W, Radek R, Brune A (2010) Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environ Microbiol 12:2120–2132Google Scholar
  106. 106.
    Hongoh Y, Sato T, Dolan MF, Noda S, Ui S, Kudo T, Ohkuma M (2007) The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the “Synergistes” group. Appl Environ Microbiol 73:6270–6276PubMedGoogle Scholar
  107. 107.
    Hongoh Y, Sato T, Noda S, Ui S, Kudo T, Ohkuma M (2007) Candidatus Symbiothrix dinenymphae: bristle-like Bacteroidales ectosymbionts of termite gut protists. Environ Microbiol 9:2631–2635PubMedGoogle Scholar
  108. 108.
    Cleveland LR, Grimstone AV (1964) The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Proc R Soc Lond B 159:668–686Google Scholar
  109. 109.
    Iida T, Ohkuma M, Ohtoko K, Kudo T (2000) Symbiotic spirochetes in the termite hindgut: phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiol Ecol 34:17–26PubMedGoogle Scholar
  110. 110.
    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 69:625–633PubMedGoogle Scholar
  111. 111.
    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 71:8811–8817PubMedGoogle Scholar
  112. 112.
    Noda S, Kitade O, Inoue T, Kawai M, Kanuka M, Hiroshima K, Hongoh Y, Constantino R, Uys V, Zhong J-H, Kudo T, Ohkuma M (2007) Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol Ecol 16:1257–1266PubMedGoogle Scholar
  113. 113.
    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 71:1473–1479PubMedGoogle Scholar
  114. 114.
    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 60:467–476PubMedGoogle Scholar
  115. 115.
    Ikeda-Ohtsubo W, Desai M, Stingl U, Brune A (2007) Phylogenetic diversity of ‘Endomicrobia’ and their specific affiliation with termite gut flagellates. Microbiology 153:3458–3465PubMedGoogle Scholar
  116. 116.
    Ikeda-Ohtsubo W, Brune A (2009) Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Mol Ecol 18:332–342PubMedGoogle Scholar
  117. 117.
    Ohkuma M, Kudo T (1996) Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl Environ Microbiol 62:461–468PubMedGoogle Scholar
  118. 118.
    Fröhlich J, König H (1999) Rapid isolation of single microbial cells from mixed natural and laboratory populations with the aid of a micromanipulator. Syst Appl Microbiol 22:249–257PubMedGoogle Scholar
  119. 119.
    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 11:1007–1015PubMedGoogle Scholar
  120. 120.
    Brune A, Stingl U (2006) Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis. Prog Mol Subcell Biol 41:39–60PubMedGoogle Scholar
  121. 121.
    Ohkuma M (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16:345–352PubMedGoogle Scholar
  122. 122.
    Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M (2008) Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci USA 105:5555–5560PubMedGoogle Scholar
  123. 123.
    Hongoh Y, Sharma VK, Prakash T, Noda S, Toh H, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M (2008) Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322:1108–1109PubMedGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  1. 1.Department of Biological Sciences, Graduate School of Bioscience and BiotechnologyTokyo Institute of TechnologyTokyoJapan

Personalised recommendations