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Termite Gut Microbiome

  • Navodita MauriceEmail author
  • László Erdei
Chapter
Part of the Sustainability in Plant and Crop Protection book series (SUPP)

Abstract

Termites depend on their gut microbes for digestion of complex polysaccharides of wood into simpler molecules. Cellulose is a major polymeric carbohydrate present in the wood which is broken down to simpler byproducts through metabolic steps by the hindgut microbes. Termite gut microbes also produce gases during the cellulose degradation process, of which methane is the major product. Gut microbes belong to three major groups, namely, bacteria, archaea and protozoa. They show a mutualistic relationship and typically convert 95% of cellulose into simple sugars within 24 h. More than 200 species of microbes form this community, producing different types of wood-busting enzymes, mainly cellulases, cellubiases, hemicellulases, glucosidases and gluconases, during wood degradation. Studies suggest that lower termites utilize both endogenous and protozoal enzymes for cellulose digestion, while higher termites acquire enzymes from their diet instead of protozoal enzymes. Some termite species change their feeding habits with seasonal variations. These affect gut microbes population and therefore are responsible for enhancing their survival under changed environmental conditions.

Keywords

Gut Microbes Cellulose Enzymes 

References

  1. Aanen, D. K., Eggleton, P., Rouland-Lefevre, C., Guldberg-Frøslev, T., Rosendahl, S., & Boomsma, J. J. (2002). The evolution of fungus growing termites and their mutualistic fungal symbionts. Proceedings of the National Academy of Sciences of the United States of America, 99, 14887–14892.PubMedPubMedCentralGoogle Scholar
  2. Aanen, D. K., Ros, V. I. D., Licht, H. H. D., Mitchell, J., de Beer, Z. W., Slippers, B., Rouland-Lefevre, C., & Boomsma, J. J. (2007). Patterns of interaction specificity of fungus-growing termites and Termitomyces symbionts in South Africa. BMC Evolutionary Biology, 7, 115.PubMedPubMedCentralGoogle Scholar
  3. Abe, Y., Bignell, D. E., & Higashi, M. (2000). Termites: Evolution, sociality, symbioses, ecology (p. 466). Dordrecht: Kluwer Academic Publishers.Google Scholar
  4. Baena, S., Fardeau, M. L., Labat, M., Ollivier, B., Thomas, P., Garcia, J. L., & Patel, B. K. (1998). Aminobacterium colombiense sp. nov., an amino-acid-degrading anaerobe isolated from anaerobic sludge. Anaerobe, 4, 241–250.PubMedGoogle Scholar
  5. Baena, S., Fardeau, M. L., Ollivier, B., Labat, M., Thomas, P., Garcia, J. L., & Patel, B. K. (1999a). Aminomonas paucivorans gen. nov., sp. nov., a mesophilic, anaerobic, amino-acid-utilizing bacterium. International Journal of Systematic Bacteriology, 49, 975–982.PubMedGoogle Scholar
  6. Baena, S., Fardeau, M. L., Woo, T. H., Ollivier, B., Labat, M., & Patel, B. K. (1999b). Phylogenetic relationships of three amino-acid-utilizing anaerobes, Selenomonas acidaminovorans, ‘Selenomonas acidaminophila’ and Eubacterium acidaminophilum, as inferred from partial 16S rDNA nucleotide sequences and proposal of Thermanaerovibrio acidaminovorans gen. nov., comb. nov. and Anaeromusa acidaminophila gen. nov., comb. nov. International Journal of Systematic Bacteriology, 49, 969–974.PubMedGoogle Scholar
  7. Baena, S., Fardeau, M. L., Labat, M., Ollivier, B., Garcia, J. L., & Patel, B. K. (2000). Aminobacterium mobile sp. nov., a new anaerobic amino-acid-degrading bacterium. International Journal of Systematic and Evolutionary Microbiology, 50, 259–264.PubMedGoogle Scholar
  8. Bandi, C., Sironi, M., Damiani, G., Magrassi, L., Nalepa, C. A., Laudani, U., & Sacchi, L. (1995). The establishment of intracellular symbiosis in an ancestor of cockroaches and termite. Proceedings of the Royal Society of London – Series B: Biological Sciences, 259, 293–299.PubMedGoogle Scholar
  9. Bauer, S., Tholen, A., Overmann, J., & Brune, A. (2000). Characterization of abundance and diversity of lactic acid bacteria in the hindgut of wood- and soil-feeding termites by molecular and culture dependent techniques. Archives of Microbiology, 173, 126–173.PubMedGoogle Scholar
  10. Berchtold, M., Ludwig, W., & Konig, H. (1994). 16S rDNA sequence and phylogenetic position of an uncultivated spirochete from the hindgut of the termite Mastotermes darwiniensis Froggatt. FEMS Microbiology Letters, 123, 269–273.PubMedGoogle Scholar
  11. Bignell, D. E. (1994). Soil-feeding and gut morphology in higher termites. In J. H. Hunt & C. A. Nalepa (Eds.), Nourishment and evolution in insect societies (pp. 131–158). Boulder: Westview Press.Google Scholar
  12. Bignell, D. E. (2000). Introduction to symbiosis. In T. Abe, D. E. Bignell, & M. Higashi (Eds.), Termites: Evolution, sociality, symbioses, ecology (pp. 189–208). Dordrecht: Kluwer Academic Publishers.Google Scholar
  13. Bignell, D. E., & Eggleton, P. (2000). Termites in ecosystems. In T. Abe, D. E. Bignell, & M. Higashi (Eds.), Termites: Evolution, sociality, symbiosis, ecology (pp. 363–387). Dordrecht: Kluwer Academic Publishers.Google Scholar
  14. Bloodgood, R. A., & Fitzharris, T. P. (1976). Specific associations of prokaryotes with symbiotic flagellate protozoa from the hindgut of the termite Reticulitermes and the wood-eating roach Cryptocercus. Cytobios, 17, 103–122.PubMedGoogle Scholar
  15. Boga, H., & Brune, A. (2003). Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Applied and Environmental Microbiology, 69, 779–786.PubMedPubMedCentralGoogle Scholar
  16. Brauman, A., Kane, M. D., Labat, M., & Breznak, J. A. (1992). Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science, 257, 1384–1387.PubMedGoogle Scholar
  17. Braun, S. T., Proctor, L. M., Zani, S., Mellon, M. T., & Zehr, J. P. (1999). Molecular evidence for zooplankton-associated nitrogen-fixing anaerobes based on amplification of the nifH gene. FEMS Microbiology Ecology, 28, 273–279.Google Scholar
  18. Breznak, J. A. (1975). Symbiotic relationships between termites and their intestinal microbiota. In D. H. Jennings & D. L. Lee (Eds.), Symbiosis (Society for experimental biology symposium ser., no. 29) (pp. 559–580). Cambridge: Cambridge University Press.Google Scholar
  19. Breznak, J. A. (1984). Biochemical aspects of symbiosis between termites and their intestinal microbiota. In J. M. Anderson, A. D. M. Rayner, & D. W. H. Walton (Eds.), Invertebrate microbial interactions (pp. 173–203). London: Cambridge University Press.Google Scholar
  20. Breznak, J. A. (1994). Acetogenesis from carbon dioxide in termite guts. In H. L. Drake (Ed.), Acetogenesis (pp. 303–330). New York: Chapman and Hall.Google Scholar
  21. Breznak, J. A. (2000). Ecology of prokaryotic microbes in the guts of wood- and litter-feeding termites. In T. Abe, D. E. Bignell, & M. Higashi (Eds.), Termites: Evolution, sociality, symbiosis, ecology (pp. 209–231). Dordrecht: Kluwer Academic Publishers.Google Scholar
  22. Breznak, J. A. (2002). Phylogenetic diversity and physiology of termite gut spirochetes. Integrative and Comparative Biology, 42, 313–318.PubMedGoogle Scholar
  23. Breznak, J. A., & Blum, J. S. (1991). Mixotrophy in the termite gut acetogen, Sporomusa termitida. Archives of Microbiology, 156, 105–110.Google Scholar
  24. Breznak, J. A., & Brune, A. (1994). Role of microorganisms in the digestion of lignocellulose by termites. Annual Review of Entomology, 39, 453–487.Google Scholar
  25. Breznak, J. A., & Switzer, J. M. (1986). Acetate synthesis from H2 plus CO2 by termite gut microbes. Applied and Environmental Microbiology, 52, 623–630.PubMedPubMedCentralGoogle Scholar
  26. Brugerolle, G. (2005). The amoeboid parabasalid flagellate Gigantomonas herculea of the African termite Hodotermes mossambicus reinvestigated using immunological and ultrastructural techniques. Acta Protozoologica, 44, 189–199.Google Scholar
  27. Brune, A. (2007). Microbiology: Woodworker’s digest. Nature, 450, 487–488.PubMedGoogle Scholar
  28. Brune, A. (2014). The family Elusimicrobiaceae. In E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, & F. Thompson (Eds.), The prokaryotes (Vol. 11., 4th ed, pp. 637–640). Berlin: Springer Verlag.Google Scholar
  29. Brune, A., & Friedrich, M. (2000). Microecology of the termite gut: Structure and function on a microscale. Current Opinion in Microbiology, 3, 263–269.PubMedGoogle Scholar
  30. Brune, A., & Kuhl, M. (1996). pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. Journal of Insect Physiology, 42, 1121–1127.Google Scholar
  31. Brune, A., & Ohkuma, M. (2011). Role of the termite gut microbiota in symbiotic digestion. In D. E. Bignell, Y. Roisin, & N. Lo (Eds.), Biology of termites: A modern synthesis (pp. 439–475). Dordrecht: Springer.Google Scholar
  32. Brune, A., Emerson, D., & Breznak, J. A. (1995). The termite gut microflora as an oxygen sink: Microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Applied and Environmental Microbiology, 61, 2681–2687.PubMedPubMedCentralGoogle Scholar
  33. Burnum, K. E., Callister, S. J., Nicora, C. D., Purvine, S. O., Hugenholtz, P., Warnecke, F., Scheffrahn, R. H., Smith, R. D., & Lipton, M. S. (2011). Proteome insights into the symbiotic relationship between a captive colony of Nasutitermes corniger and its hindgut microbiome. The ISME Journal, 5, 161–164.PubMedGoogle Scholar
  34. Canale-Parola, E. (1984). Order I. Spirochaetales Buchanan 1917, 163AL. In N. R. Krieg & J. G. Holt (Eds.), Bergey’s manual of systematic bacteriology (pp. 38–39). Baltimore: Williams & Wilkins.Google Scholar
  35. Cavalier-Smith, T. (2002). The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology, 52, 297–354.PubMedGoogle Scholar
  36. Charon, N. W., Greenberg, E. P., Koopman, M. B., & Limberger, R. J. (1992). Spirochaete chemotaxis, motility, and the structure of the spirochetal periplasmic flagella. Research in Microbiology, 143, 597–603.PubMedGoogle Scholar
  37. Chen, J. S. (1995). Alcohol dehydrogenase: Multiplicity and relatedness in the solvent-producing clostridia. FEMS Microbiology Reviews, 17, 263–273.PubMedGoogle Scholar
  38. Chiang, V. L., & Funaoka, M. (1990). The difference between guaiacyl and guaiacyl-syringyl lignins in their responses to kraft delignification. Holzforschung, 44, 309–313.Google Scholar
  39. Chien, Y. T., & Zinder, S. H. (1996). Cloning, functional organization, transcript studies, and phylogenetic analysis of the complete nitrogenase structural genes (nifHDK2) and associated genes in the archaeon Methanosarcina barkeri. Journal of Bacteriology, 178, 143–148.PubMedPubMedCentralGoogle Scholar
  40. Cleveland, L. R. (1926). Symbiosis among animals with special reference to termites and their intestinal flagellates. The Quarterly Review of Biology, 1, 51–64.Google Scholar
  41. Cleveland, L. R., & Grimstone, A. V. (1964). The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Proceedings of the Royal Society of London. Series B, Biological Sciences, 159, 668–686.Google Scholar
  42. Cranshaw, W. (2013). Bugs rule: An introduction to the world of insects (p. 188). Princeton: Princeton University Press.Google Scholar
  43. Cummings, J. H., & Macfarlane, G. T. (1997). Role of intestinal bacteria in nutrient metabolism. JPEN, 21, 357–365.Google Scholar
  44. Czolij, R., Slaytor, M., & O’Brien, R. W. (1985). Bacterial flora of the mixed segment and the hindgut of the higher termite Nasutitermes exitiosus Hill (Termitidae, Nasutitermitinae). Applied and Environmental Microbiology, 49, 1226–1236.Google Scholar
  45. Darlington, J. E. C. P. (1994). Nutrition and evolution in fungus-growing ants. In J. H. Hunt & C. A. Nalepa (Eds.), Nourishment and evolution in insect societies (pp. 105–130). Boulder: Westview Press.Google Scholar
  46. Davis, E. C., Franklin, J. B., Shaw, A. J., & Vilgalys, R. (2003). Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: Phylogenetics, distribution, and symbiosis. American Journal of Botany, 90, 1661–1667.PubMedGoogle Scholar
  47. De Fine Licht, H. H., Andersen, A., & Aanen, D. K. (2005). Termitomyces sp. associated with the termite Macrotermes natalensis has a heterothallic mating system and multinucleate cells. Mycological Research, 109, 314–318.PubMedGoogle Scholar
  48. Dean, D. R., & Jacobson, M. R. (1992). Biochemical genetics of nitrogenase. In G. Stacy, R. H. Burris, & H. J. Evans (Eds.), Biological nitrogen fixation (pp. 763–834). New York: Chapman and Hall.Google Scholar
  49. Delalibera, I., Handelsman, J., & Raffa, K. F. (2005). Contrasts in cellulolytic activities of gut microorganisms between the wood borer, Saperda vestita (Coleoptera: Cerambycidae) and the bark beetles, Ips pini and Dendroctonus frontalis (Coleoptera: Curculionidae). Environmental Entomology, 34, 541–547.Google Scholar
  50. Dietrich, C., Kohler, T., & Brune, A. (2014). The cockroach origin of the termite gut microbiota: Patterns in bacterial community structure reflect major evolutionary events. Applied and Environmental Microbiology, 80, 2261–2269.PubMedPubMedCentralGoogle Scholar
  51. Donovan, S. E., Purdy, K. J., Kane, M. D., & Eggleton, P. (2004). Comparison of Euryarchaea strains in the guts and food-soil of the soil-feeding termite Cubitermes fungifaber across different soil types. Applied and Environmental Microbiology, 70, 3884–3892.PubMedPubMedCentralGoogle Scholar
  52. Dow, J. A. T. (1986). Insect midgut function. Advances in Insect Physiology, 19, 188–328.Google Scholar
  53. Droge, S., Rachel, R., Radek, R., & Konig, H. (2008). Treponema isoptericolens sp. nov., a novel spirochaete from the hindgut of the termite Incisitermes tabogae. International Journal of Systematic and Evolutionary Microbiology, 58, 1079–1083.PubMedGoogle Scholar
  54. 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). Applied and Environmental Microbiology, 63, 4039–4046.PubMedPubMedCentralGoogle Scholar
  55. Engel, M. S., Grimaldi, D. A., & Krishna, K. (2009). Termites (Isoptera): Their phylogeny, classification, and rise to ecological dominance. American Museum Novitates, 3650, 1–27.Google Scholar
  56. Esenther, G. R., & Kirk, T. K. (1974). Catabolism of aspen sapwood in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Annals of the Entomological Society of America, 67, 989–991.Google Scholar
  57. Filley, T. R. (2003). In B. Goodell, D. D. Nicholas, & T. P. Schultz (Eds.), ACS symposium series in wood deterioration and preservation: Advances in our changing world (pp. 119–139). Washington, DC: American Chemical Society.Google Scholar
  58. Filley, T. R., Hatcher, P. G., Shortle, W. C., & Praseuth, R. T. (2000). The application of 13C-labeled tetramethylammonium hydroxide (13C-TMAH) thermochemolysis to the study of fungal degradation of wood. Organic Geochemistry, 31, 181–198.Google Scholar
  59. Filley, T. R., Nierop, K. G. J., & Wang, Y. (2006). The contribution of polyhydroxyl aromatic compounds to tetramethylammonium hydroxide lignin-based proxies. Organic Geochemistry, 37, 711–727.Google Scholar
  60. Frank, S. A. (1996). Host-symbiont conflict over the mixing of symbiotic lineages. Proceedings of the Royal Society of London B: Biological Sciences, 263, 339–344.Google Scholar
  61. Frohlich, J., Sass, H., Babenzien, H.-D., Kuhnigk, T., Varma, A., Saxena, S., Nalepa, C., Pfeiffer, P., & Konig, H. (1999). Isolation of Desulfovibrio intestinalis sp. nov. from the hindgut of the lower termite Mastotermes darwiniensis. Canadian Journal of Microbiology, 45, 145–152.PubMedGoogle Scholar
  62. Fuhrman, J. A., McCallum, K., & Davis, A. A. (1993). Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans. Applied and Environmental Microbiology, 59, 1294–1302.PubMedPubMedCentralGoogle Scholar
  63. Fuller, C. A. (2007). Fungistatic activity of freshly killed termite, Nasutitermes acajutlae, soldiers in the Caribbean. Journal of Insect Science, 7, 14.PubMedCentralGoogle Scholar
  64. Gerbod, D., Sanders, E., Moriya, S., Noel, C., Takasu, H., Fast, N. M., Delgado-Viscogliosi, P., Ohkuma, M., Kudo, T., Capron, M., Palmer, J. D., Keeling, P. J., & Viscogliosi, E. (2004). Molecular phylogenies of Parabasalia inferred from four protein genes and comparison with rRNA trees. Molecular Phylogenetics and Evolution, 31, 572–580.PubMedGoogle Scholar
  65. Godon, J.-J., Moriniere, J., Moletta, M., Gaillac, M., Bru, V., & Delgenes, J.-P. (2005). Rarity associated with specific ecological niches in the bacterial world: The ‘Synergistes’ example. Environmental Microbiology, 7, 213–224.PubMedGoogle Scholar
  66. Graber, J. R., & Breznak, J. A. (2000). Nutrition and physiological properties of termite gut spirochaetes. Abstracts of the American Society for Microbiology no. N-104.Google Scholar
  67. Graber, J. R., Leadbetter, J. R., & Breznak, J. A. (2004). Description of Treponema azonutricum sp. nov and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Applied and Environmental Microbiology, 70, 1307–1314.PubMedPubMedCentralGoogle Scholar
  68. Grimaldi, D. (2001). Insect evolutionary history from Handlirsch to Hennig, and beyond. Journal of Paleontology, 75, 1152–1160.Google Scholar
  69. He, S., Ivanova, N., Kirton, E., Allgaier, M., Bergin, C., Scheffrahn, R. H., Kyrpides, N. C., Warnecke, F., Tringe, S. G., & Hugenholtz, P. (2013). Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood- and dung-feeding higher termites. PLoS One, 8, e61126.PubMedPubMedCentralGoogle Scholar
  70. Herre, E. A., Mejia, L. C., Kyllo, D. A., Rojas, E., Maynard, Z., Butler, A., & Van Bael, S. A. (2007). Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology, 88, 550–558.PubMedGoogle Scholar
  71. Hethener, P., Braumann, A., & Garcia, J.-L. (1992). Clostridium termitidis sp. nov., a cellulolytic bacterium from the gut of the wood feeding termite, Nasutitermes lujae. Systematic and Applied Microbiology, 15, 52–58.Google Scholar
  72. Higashi, M., & Abe, T. (1997). Global diversification of termites driven by the evolution of symbiosis and sociality. In T. Abe, S. A. Levin, & M. Higashi (Eds.), Biodiversity: An ecological perspective (pp. 83–112). New York: Springer-Verlag.Google Scholar
  73. Hongoh, Y. (2010). Diversity and genomes of uncultured microbial symbionts in the termite gut. Bioscience, Biotechnology, and Biochemistry, 74, 1145–1151.PubMedGoogle Scholar
  74. Hongoh, Y. (2011). Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cellular and Molecular Life Sciences, 68, 1311–1325.PubMedGoogle Scholar
  75. Hongoh, Y., Ohkuma, M., & Kudo, T. (2003). Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiology Ecology, 44, 231–242.PubMedGoogle Scholar
  76. Hongoh, Y., Deevong, P., Hattori, S., Inoue, T., Noda, S., Noparatnaraporn, N., Kudo, T., & Ohkuma, M. (2006). Phylogenetic diversity, localization and cell morphologies of the candidate phylum TG3 and a subphylum in the phylum Fibrobacteres, recently found bacterial groups dominant in termite guts. Applied and Environmental Microbiology, 72, 6780–6788.PubMedPubMedCentralGoogle Scholar
  77. Horn, M., Harzenetter, M. D., Linner, T., Schmid, E. N., Muller, K.-D., Michel, R., & Wagner, M. (2001). Members of the Cytophaga-Flavobacterium-Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of ‘Candidatus Amoebophilus asiaticus.’. Environmental Microbiology, 3, 440–449.PubMedGoogle Scholar
  78. Huang, X. F., Bakker, M. G., Judd, T. M., Reardon, K. F., & Vivanco, J. M. (2013). Variations in diversity and richness of gut bacterial communities of termites (Reticulitermes flavipes) fed with grassy and woody plant substrates. Microbial Ecology, 65, 531–536.PubMedGoogle Scholar
  79. Hungate, R. E. (1946). Studies on cellulose fermentation. II. An anaerobic cellulose-decomposing actinomycete, Micromonospora propionici, n. sp. Journal of Bacteriology, 51, 51–56.PubMedCentralGoogle Scholar
  80. Husseneder, C. (2010). Symbiosis in subterranean termites: A review of insights from molecular studies. Environmental Entomology, 39, 378–388.PubMedGoogle Scholar
  81. Hyodo, F., Inoue, T., Azuma, J. I., Tayasu, I., & Abe, T. (2000). Role of the mutualistic fungus in lignin degradation in the fungus-growing termite Macrotermes gilvus (Isoptera; Macrotermitinae). Soil Biology and Biochemistry, 32, 653–658.Google Scholar
  82. Hyodo, F., Tayasu, I., Inoue, T., Azuma, J.-I., Kudo, T., & Abe, T. (2003). Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Functional Ecology, 17, 186–193.Google Scholar
  83. Iida, T., Ohkuma, M., Ohtoko, K., & Kudo, T. (2000). Symbiotic spirochetes in the termite hindgut: Phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiology Ecology, 34, 17–26.PubMedGoogle Scholar
  84. Ikeda-Ohtsubo, W., & Brune, A. (2009). Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Molecular Ecology, 18, 332–342.PubMedGoogle Scholar
  85. Inoue, T., Murashima, K., Azuma, J.-I., Sugimoto, A., & Slaytor, M. (1997). Cellulose and xylan utilisation in the lower termite Reticulitermes speratus. Journal of Insect Physiology, 43, 235–242.PubMedGoogle Scholar
  86. Inoue, T., Kitade, O., Yoshimura, T., & Yamaoka, I. (2000). Symbiotic associations with protists. In T. Abe, D. E. Bignell, & M. Higashi (Eds.), Termites: Evolution, sociality, symbioses, ecology (pp. 275–288). Dordrecht: Kluwer Academic Publishers.Google Scholar
  87. Inward, D., Beccaloni, G., & Eggleton, P. (2007). Death of an order: A comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biology Letters, 3, 331–335.PubMedPubMedCentralGoogle Scholar
  88. Johjima, T., Taprab, Y., Noparatnaraporn, N., Kudo, T., & Ohkuma, M. (2006). Large-scale identification of transcripts expressed in a symbiotic fungus (Termitomyces) during plant biomass degradation. Applied Microbiology and Biotechnology, 73, 195–203.PubMedGoogle Scholar
  89. Johnson, R. A. (1981). Colony development and establishment of the fungus comb in Microtermes sp. nr. Usambaricus (Sjöst) (Isoptera, Macrotermitinae) from Nigeria. Insectes Sociaux, 28, 3–12.Google Scholar
  90. Kane, M. D., & Breznak, J. A. (1991). Acetonema longum gen. nov. sp. nov., an H2/CO2 acetogenic bacterium from the termite, Pterotermes occidentis. Archives of Microbiology, 156, 91–98.PubMedGoogle Scholar
  91. Kane, M. D., Brauman, A., & Breznak, J. A. (1991). Clostridium mayombei sp. nov., an H2/CO2 acetogenic bacterium from the gut of the African soil-feeding termite, Cubitermes speciosus. Archives of Microbiology, 156, 99–104.Google Scholar
  92. Kappler, A. (1999). Influence of gut alkalinity and oxygen status on mobilization and size-class distribution of humic acids in the hindgut of soil-feeding termites. Applied Soil Ecology, 13, 3.Google Scholar
  93. Katoh, H., Miura, T., Maekawi, K., Shinzato, N., & Matsumoto, T. (2002). Genetic variation of symbiotic fungi cultivated by the macrotermitine termite Odontotermes formosanus (Isoptera: Termitidae) in the Ryukyu Archipelago. Molecular Ecology, 11, 1565–1572.PubMedGoogle Scholar
  94. Katsumata, K. S., Jin, Z. F., Hori, K., & Iiyama, K. (2007). Structural changes in lignin of tropical woods during digestion by termite, Cryptotermes brevis. Journal of Wood Science, 53, 419–426.Google Scholar
  95. Katzin, L. I., & Kirby, H. (1939). The relative weight of termites and their protozoa. The Journal of Parasitology, 25, 444–445.Google Scholar
  96. Khalil, M. A. K., Rasmussen, R. A., French, J. R., & Holt, J. (1990). The influence of termites on atmospheric trace gases: CH4, CO2, CHCl3, N2O, CO, H2, and light hydrocarbons. Journal of Geophysical Research, 95, 3619–3634.Google Scholar
  97. Kirk, P. M., Canno, P. F., David, J. C., & Stalpers, J. A. (2001). Ainsworth & Bigby’s dictionary of the fungi. Wallingford: CAB International.Google Scholar
  98. Kirshtein, J. D., Paerl, H. W., & Zehr, J. (1991). Amplification, cloning, and sequencing of a nifH segment from aquatic microorganisms and natural communities. Applied and Environmental Microbiology, 57, 2645–2650.PubMedPubMedCentralGoogle Scholar
  99. Kitade, O., Maeyama, T., & Matsumoto, T. (1997). Establishment of symbiotic flagellate fauna of Hodotermopsis japonica (Isoptera: Termopsidae). Sociobiology, 30, 161–167.Google Scholar
  100. Korb, J., & Linsenmair, K. E. (2000a). Thermoregulation of termite mounds: What role does ambient temperature and metabolism of the colony play? Insectes Sociaux, 47, 357–363.Google Scholar
  101. Korb, J., & Linsenmair, K. E. (2000b). Ventilation of termite mounds: New results require a new model. Behavioral Ecology, 11, 486–494.Google Scholar
  102. Krasil’nikov, N. A., & Satdykov, S. I. (1970). Bacteria of termites’ intestines. Microbiology, 39, 562–564.Google Scholar
  103. Kudo, T., Ohkuma, M., Moriya, S., Noda, S., & Ohtoko, K. (1998). Molecular phylogenetic identification of the intestinal anaerobic microbial community in the hindgut of the termite, Reticulitermes speratus, without cultivation. Extremophiles, 2, 155–161.PubMedGoogle Scholar
  104. Kuhnigk, T., Branke, J., Krekeler, D., Cypionka, H., & Konig, H. (1996). A feasible role of sulfate-reducing bacteria in the termite gut. Systematic and Applied Microbiology, 19, 139–149.Google Scholar
  105. Kukor, J., Cowan, D., & Martin, M. (1988). The role of ingested fungal enzymes in cellulose digestion in the larvae of cerambycid beetles. Physiological Zoology, 61, 364–371.Google Scholar
  106. Leadbetter, J. R., & Breznak, J. A. (1996). Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes. Applied and Environmental Microbiology, 62, 3620–3631.PubMedPubMedCentralGoogle Scholar
  107. Leadbetter, J. R., Crosby, L. D., & Breznak, J. A. (1998). Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts. Archives of Microbiology, 169, 287–292.PubMedGoogle Scholar
  108. Leadbetter, J. R., Schmidt, T. M., Graber, J. R., & Breznak, J. A. (1999). Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science, 283, 686–689.PubMedGoogle Scholar
  109. Leidy, J. (1877). On the intestinal parasites of Termes flavipes. Proceedings of the Academy of Natural Sciences (Philadelphia), 29, 146–149.Google Scholar
  110. Leidy J (1874–1881) The parasites of the termites. Journal of the Academy of Natural Sciences (Philadelphia) 8, 425–447.Google Scholar
  111. Li, Z. Q., Liu, B. R., Zeng, W. H., Xiao, W. L., Li, Q. J., & Zhong, J. H. (2013). Character of cellulase activity in the guts of flagellate-free termites with different feeding habits. Journal of Insect Science, 13, 1–8.Google Scholar
  112. Lilburn, T. G., Kim, K. S., Ostrom, N. E., Byzek, K. R., Leadbetter, J. R., & Breznak, J. A. (2001). Nitrogen fixation by symbiotic and free-living spirochaetes. Science, 292, 2495–2498.PubMedGoogle Scholar
  113. Liu, N., Zhang, L., Zhou, H., Zhang, M., Yan, X., Wang, Q., Long, Y., Xie, L., Wang, S., Huang, Y., & Zhou, Z. (2013). Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). PLoS One, 8, e69184.PubMedPubMedCentralGoogle Scholar
  114. Lo, N. (2003). Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Molecular Biology and Evolution, 20, 907–913.PubMedGoogle Scholar
  115. Makonde, H. M., Boga, H. I., Osiemo, Z., Mwirichia, R., Mackenzie, L. M., Goker, M., & Klenk, H. P. (2013). 16S-rRNA-based analysis of bacterial diversity in the gut of fungus-cultivating termites (Microtermes and Odontotermes species). Antonie van Leeuwenhoek, 104, 869–883.PubMedGoogle Scholar
  116. Mauldin, J. K. (1977). Cellulose catabolism and lipid synthesis by normally and abnormally faunated termites, Reticulitermes flavipes. Insect Biochemistry, 7, 27–31.Google Scholar
  117. Mikaelyan, A., Strassert, J. F. H., Tokuda, G., & Brune, A. (2014). The fiber-associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites (Nasutitermes spp.) Environmental Microbiology, 16, 2711–2722.Google Scholar
  118. Moriya, S., Dacks, J. B., Takagi, A., Noda, S., Ohkuma, M., Doolittle, W. F., & Kudo, T. (2003). Molecular phylogeny of three oxymonad genera: Pyrsonympha, Dinenympha and Oxymonas. The Journal of Eukaryotic Microbiology, 50, 190–197.PubMedGoogle Scholar
  119. Mueller, U. G., Schultz, T. R., Currie, C. R., Adams, R. M. M., & Malloch, D. (2001). The origin of the attine ant-fungus mutualism. The Quarterly Review of Biology, 76, 169–197.PubMedGoogle Scholar
  120. Nalepa, C. A., Bignell, D. E., & Bandi, C. (2001). Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insectes Sociaux, 48, 194–201.Google Scholar
  121. Nobre, T., Rouland-Lefevre, C., & Aanen, D. K. (2011). Comparative biology of fungus cultivation in termites and ants. In D. Bignell, Y. Roisin, & N. Lo (Eds.), Biology of termites: A modern synthesis (pp. 193–210). Dordrecht: Springer.Google Scholar
  122. 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. Applied and Environmental Microbiology, 65, 4935–4942.PubMedPubMedCentralGoogle Scholar
  123. 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. Applied and Environmental Microbiology, 69, 625–633.PubMedPubMedCentralGoogle Scholar
  124. 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 Evolutionary Biology, 9, 158.PubMedPubMedCentralGoogle Scholar
  125. Noirot, C., & Noirot-Timothee, C. (1969). The digestive system. In K. Krishna & F. M. Weesner (Eds.), Biology of termites (pp. 49–88). New York: Academic Press.Google Scholar
  126. O’Brien, R. W., & Slaytor, M. (1982). Role of microorganisms in the metabolism of termites. Australian Journal of Biological Sciences, 35, 239–262.Google Scholar
  127. Odelson, D. A., & Breznak, J. A. (1983). Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Applied and Environmental Microbiology, 45, 1602–1613.PubMedPubMedCentralGoogle Scholar
  128. Ohkuma, M. (1998). Phylogenetic analysis of the symbiotic intestinal microflora of the termite Cryptotermes domesticus. FEMS Microbiology Letters, 164, 389–395.Google Scholar
  129. Ohkuma, M. (2003). Termite symbiotic systems: Efficient bio-recycling of lignocellulose. Applied Microbiology and Biotechnology, 61, 1–9.PubMedGoogle Scholar
  130. Ohkuma, M., & Brune, A. (2011). Diversity, structure, and evolution of the termite gut microbial community. In D. E. Bignell, Y. Roisin, & N. Lo (Eds.), Biology of termites: A modern synthesis (pp. 413–438). Dordrecht: Springer.Google Scholar
  131. Ohkuma, M., & Kudo, T. (1996). Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Applied and Environmental Microbiology, 62, 461–468.PubMedPubMedCentralGoogle Scholar
  132. Ohkuma, M., Noda, S., Usami, R., Horikoshi, K., & Kudo, T. (1996). Diversity of nitrogen fixation genes in the symbiotic intestinal microflora of the termite Reticulitermes speratus. Applied and Environmental Microbiology, 62, 2747–2752.PubMedPubMedCentralGoogle Scholar
  133. Ohkuma, M., Noda, S., & Kudo, T. (1999). Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Applied and Environmental Microbiology, 65, 4926–4934.PubMedPubMedCentralGoogle Scholar
  134. 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. Molecular Phylogenetics and Evolution, 31, 701–710.PubMedGoogle Scholar
  135. Ohkuma, M., Iida, T., Ohtoko, K., Yuzawa, H., Noda, S., Viscogliosi, E., & Kudo, T. (2005). Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Hypermastigea. Molecular Phylogenetics and Evolution, 35, 646–655.PubMedGoogle Scholar
  136. Ohkuma, M., Noda, S., Hongoh, Y., Nalepa, C. A., & Inoue, T. (2009). Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proceedings of the Royal Society of London – Series B: Biological Sciences, 276, 239–245.PubMedGoogle Scholar
  137. Osono, T., & Takeda, H. (1999). Decomposing ability of interior and surface fungal colonizers of beech leaves with reference to lignin decomposition. European Journal of Soil Biology, 35, 51–56.Google Scholar
  138. Paster, B. J., Dewhirst, F. E., Weisburg, W. G., Tordoff, L. A., Fraser, G. J., Hespell, R. B., Stanton, T. B., Zablen, L., Mandelco, L., & Woese, C. R. (1991). Phylogenetic analysis of the spirochetes. Journal of Bacteriology, 173, 6101–6109.PubMedPubMedCentralGoogle Scholar
  139. Paster, B. J., Dewhirst, F. E., Cooke, S. M., Fussing, V., Poulsen, L. K., & Breznak, J. A. (1996). Phylogeny of not-yet-cultured spirochetes from termite guts. Applied and Environmental Microbiology, 62, 347–352.PubMedPubMedCentralGoogle Scholar
  140. Potrikus, C. J., & Breznak, J. A. (1980). Uric acid-degrading bacteria in guts of termites [Reticulitermes flavipes (Kollar)]. Applied and Environmental Microbiology, 40, 117–124.PubMedPubMedCentralGoogle Scholar
  141. Ptacek, P., Brandstetr, J., Soukal, F., & Opravil, T. (2013). Investigation of subterranean termites nest material composition, structure and properties. In Y. Mastai (Ed.), Materials science-advanced topics. London: InTech. https://doi.org/10.5772/55145.Google Scholar
  142. Radek, R., & Nitsch, G. (2007). Ectobiotic spirochetes of flagellates from the termite Mastotermes darwiniensis: Attachment and cyst formation. European Journal of Protistology, 43, 281–294.PubMedGoogle Scholar
  143. Rainey, F. A., Ward-Rainey, N. L., Janssen, P. H., Hippe, H., & Stackebrandt, E. (1996). Clostridium paradoxum DSM 7308T contains multiple 16S rRNA genes with heterogeneous intervening sequences. Microbiology, 142, 2087–2095.PubMedGoogle Scholar
  144. Rees, G. N., Patel, B. K., Grassia, G. S., & Sheehy, A. J. (1997). Anaerobaculum thermoterrenum gen. nov., sp. nov., a novel, thermophilic bacterium which ferments citrate. International Journal of Systematic Bacteriology, 47, 150–154.PubMedGoogle Scholar
  145. Rieu-Lesme, F., Dauga, C., Morvan, O., Bouvet, P., Grimont, P. A., & Dore, J. (1996). Acetogenic coccoid spore-forming bacteria isolated from the rumen. Research in Microbiology, 147, 753–764.PubMedGoogle Scholar
  146. Rogers, J. D. (2000). Thoughts and musings on tropical Xylariaceae. Mycological Research, 104, 1412–1420.Google Scholar
  147. Rogers, J. D., YM, J., & Lehmann, J. (2005). Some Xylaria species on termite nests. Mycologia, 97, 914–923.PubMedGoogle Scholar
  148. Rouland, C., Lenoir, F., & Lepage, M. (1991). The role of the symbiotic fungus in the digestive metabolism of several species of fungus-growing termites. Comparative Biochemistry and Physiology. Part A, Physiology, 99, 657–663.Google Scholar
  149. Rouland-Lefevre, C., Diouf, M. N., Brauman, A., & Neyra, M. (2002). Phylogenetic relationships in Termitomyces (Family Agaricaceae) based on the nucleoticle sequence of ITS: A first approach to elucidate the evolutionary history of the symbiosis between fungus-growing termites and their fungi. Molecular Phylogenetics and Evolution, 22, 423–429.PubMedGoogle Scholar
  150. Sanderson, M. G. (1996). Biomass of termites and their emissions of methane and carbon dioxide: A global database. Global Biogeochem Cycles, 10, 543–557.Google Scholar
  151. Scharf, M. E., Karl, Z. J., Sethi, A., & Boucias, D. G. (2011). Multiple levels of synergistic collaboration in termite lignocellulose digestion. PLoS One, 6, e21709.PubMedPubMedCentralGoogle Scholar
  152. Schauer, C., Thompson, C. L., & Brune, A. (2012). The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Applied and Environmental Microbiology, 78, 2758–2767.PubMedPubMedCentralGoogle Scholar
  153. Schloss, P. D., Delalibera, I., Handelsman, J., & Raffa, K. F. (2006). Bacteria associated with the guts of two wood-boring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae). Environmental Entomology, 35, 625–629.Google Scholar
  154. Schmitt-Wagner, D., Friedrich, M. W., Wagner, B., & Brune, A. (2003). Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp). Applied and Environmental Microbiology, 69, 6007–6017.PubMedPubMedCentralGoogle Scholar
  155. Shah, H. N. (1992). The genus Bacteroides and related taxa. In A. Balows, H. G. Truper, M. Dworkin, W. Harder, & K. H. Schleifer (Eds.), The Prokaryotes (pp. 3593–3607). New York: Springer.Google Scholar
  156. Shary, S., Ralph, S. A., & Hammel, K. E. (2007). New insights into the ligninolytic capability of a wood decay ascomycete. Applied and Environmental Microbiology, 73, 6691–6694.PubMedPubMedCentralGoogle Scholar
  157. Shellman-Reeve, J. S. (1997). In J. C. Choe & B. J. Crespi (Eds.), Social competition and cooperation in insects and arachnids (pp. 52–93). Cambridge: Cambridge University Press.Google Scholar
  158. Shinzato, N., Matsumoto, T., Yamaoka, I., Oshima, T., & Yamagishi, A. (2001). Methanogenic symbionts and the locality of other host lower termites. Microbes and Environments, 16, 43–47.Google Scholar
  159. Shinzato, N., Muramatsu, M., Matsui, T., & Watanabe, Y. (2005). Molecular phylogenetic diversity of the bacterial community in the gut of the termite Coptotermes formosanus. Bioscience, Biotechnology, and Biochemistry, 69, 1145–1155.PubMedGoogle Scholar
  160. Sieber, R. (1983). Establishment of fungus comb in laboratory colonies of Macrotermes michaelseni and Odontotermes montanus (Isoptera, Macrotermitinae). Insectes Sociaux, 30, 204–209.Google Scholar
  161. Simpson, A. G. B. (2006). Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of “primitive” eukaryotes. Molecular Biology and Evolution, 23, 615–625.PubMedGoogle Scholar
  162. 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.PubMedGoogle Scholar
  163. Stingl, U., Radek, R., Yang, H., & Brune, A. (2005). “Endomicrobia”: Cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes. Applied and Environmental Microbiology, 71, 1473–1479.PubMedPubMedCentralGoogle Scholar
  164. Surkov, A. V., Dubinina, G. A., Lysenko, A. M., Glockner, F. O., & Kuever, J. (2001). Dethiosulfovibrio russensis sp. nov., Dethosulfovibrio marinus sp. nov. and Dethosulfovibrio acidaminovorans sp. nov., novel anaerobic, thiosulfate and sulfur-reducing bacteria from ‘Thiodendron’ sulfur mats in different saline environments. International Journal of Systematic and Evolutionary Microbiology, 51, 327–337.PubMedGoogle Scholar
  165. 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. Applied and Environmental Microbiology, 71, 7696–7704.PubMedPubMedCentralGoogle Scholar
  166. Tayasu, I., Sugimoto, A., Wada, E., & Abe, T. (1994). Xylophagous termites depending on atmospheric nitrogen. Naturwissenschaften, 81, 229–231.Google Scholar
  167. Tellam, R. L., Wijffels, G., & Willadsen, P. (1999). Peritrophic matrix proteins. Insect Biochemistry and Molecular Biology, 29, 87–101.PubMedGoogle Scholar
  168. Thayer, D. W. (1976). Facultative wood-digesting bacteria from the hind-gut of the termite Reticulitermes hesperus. Journal of General Microbiology, 95, 287–296.Google Scholar
  169. Tholen, A., & Brune, A. (1997). Location and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil feeding higher termites (Cubitermes spp). Applied and Environmental Microbiology, 65, 44975–44405.Google Scholar
  170. Tholen, A., & Brune, A. (2000). Impact of oxygen on metabolic fluxes and in situ rates of reductive acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes. Environmental Microbiology, 2, 436–449.PubMedGoogle Scholar
  171. Thorne, B. L. (1997). Evolution of eusociality in termites. Annual Review of Ecology and Systematics, 28, 27–54.Google Scholar
  172. Tokuda, G., Watanabe, H., Matsumoto, T., & Noda, H. (1997). Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): Distribution of cellulases and properties of endo-β -1,4-glucanase. Zoological Science, 14, 83–93.PubMedGoogle Scholar
  173. Tokuda, G., Yamaoka, I., & Noda, H. (2000). Localization of symbiotic clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki). Applied and Environmental Microbiology, 66, 2199–2207.PubMedPubMedCentralGoogle Scholar
  174. 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 Microbiology Ecology, 33, 233–240.PubMedGoogle Scholar
  175. Veivers, P. C., Muhlemann, R., Slaytor, M., Leuthold, R. H., & Bignell, D. E. (1991). Digestion, diet and polyethism in two fungus-growing termites: Macrotermes subhyalinus Rambur and M. michaelseni Sjostedt. Journal of Insect Physiology, 37, 675–682.Google Scholar
  176. Waller, D. A. (1988). Ecological similarities of fungus growing ants (Attini) and termites (Macrotermitinae). In J. C. Trager & E. J. Brill (Eds.), Advances in myrmecology (pp. 337–345). New York: E. J. Brill.Google Scholar
  177. Warnecke, F., Luginbuhl, P., Ivanova, N., et al. (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature, 450, 560–565.PubMedGoogle Scholar
  178. Wenzel, M., Radek, R., Brugerollec, G., & Konig, H. (2003). Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. European Journal of Protistology, 39, 11–23.Google Scholar
  179. Widmer, F., Shaffer, B. T., Porteous, L. A., & Seidler, R. J. (1999). Analysis of nifH gene pool complexity in soil and litter at a Douglas fir forest site in the Oregon Cascade mountain range. Applied and Environmental Microbiology, 65, 374–380.PubMedPubMedCentralGoogle Scholar
  180. Wood, T. G., & Thomas, R. J. (1989). The mutualistic association between Macrotermitinae and Termitomyces. In N. Wilding, N. M. Collins, P. M. Hammond, & J. F. Webber (Eds.), Insect-fungus interactions (pp. 69–92). New York: Academic Press.Google Scholar
  181. Yamaoka, I., & Nagatani, Y. (1980). Phagocytic cells in the midgut epithelium of the termite, Reticulitermes speratus (Kolbe). Zoological Magazine, 89, 308–311.Google Scholar
  182. Yamin, M. A. (1979). Termite flagellates. Sociobiology, 4, 1–119.Google Scholar
  183. Zavarzina, D. G., Zhilina, T. N., Tourova, T. P., Kuznetsov, B. B., Kostrikina, N. A., & Bonch-Osmolovskaya, E. A. (2000). Thermanaerovibrio velox sp. nov., a new anaerobic, thermophilic, organotrophic bacterium that reduces elemental sulfur, and emended description of the genus Thermanaerovibrio. International Journal of Systematic and Evolutionary Microbiology, 50, 1287–1295.PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratory of Immunology, Institute of GeneticsBiological Research Centre, Hungarian Academy of SciencesSzegedHungary
  2. 2.Department of Plant Biology, Faculty of Science and InformaticsUniversity of SzegedSzegedHungary

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