Role of the Termite Gut Microbiota in Symbiotic Digestion

Chapter

Abstract

The symbiotic gut microbiota of termites plays important roles in lignocellulose digestion and nitrogen metabolism. Termites possess a dual cellulolytic system: in lower termites the cellulases are contributed by both the insect and its gut flagellates, whereas in higher termites, host cellulases and hindgut bacteria participate in fiber digestion. Commonly, the microbial feeding chain is driven by the primary fermentations of carbohydrates. However in soil-feeding taxa, which exploit the peptidic component of soil organic matter as a dietary resource and show pronounced differences in physiochemical conditions along their highly compartmented intestinal tract, amino acids are an important substrate for the microbiota. Hydrogen appears to be the central intermediate in the hindgut fermentations in all termites. In wood-feeding taxa, it is efficiently recycled by homoacetogenic spirochetes, which prevail over methanogenic archaea probably because of their ability to colonize the bulk volume of the hindgut, whereas methanogens are restricted to particular microniches at the hindgut wall or within the gut flagellates. As a general rule, the spatial separation of microbial populations and metabolic activities gives rise to steep gradients of metabolites. The continuous influx of oxygen into the hindgut affects microbial metabolism in the microoxic periphery, and the anoxic status of the gut center is maintained only by the rapid reduction of oxygen by both aerobic and anaerobic microorganisms. Lignin is not significantly mineralized during gut passage, but modification of polyphenols by processes yet uncharacterized may increase the digestibility of both lignocellulose and humic substances. In wood-feeding termites, gut microbiota fix and upgrade nitrogen and recycle nitrogenous waste products. The microorganisms responsible for these reactions are mostly unknown, but recent studies have indicated that bacterial ectosymbionts and endosymbionts of the gut flagellates play a major role in the nitrogen metabolism of lower termites.

Keywords

nifH Gene Glycosyl Hydrolase Family Termite Species High Termite Lower Termite 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank John A. Breznak for helpful comments and Karen A. Brune for editing an earlier version of the manuscript.

References

  1. Arakawa G, Watanabe H, Yamasaki H et al (2009) Purification and molecular cloning of xylanases from the wood-feeding termite, Coptotermes Formosanus Shiraki. Biosci Biotechnol Biochem 73:710–718PubMedCrossRefGoogle Scholar
  2. Azuma J, Nishimoto K, Koshijima T (1984) Studies on digestive system of termites. II. Properties of carbohydrolases of termite Coptotermes formosanus Shiraki. Wood Res 70:1–16Google Scholar
  3. 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. Arch Microbiol 173:126–173PubMedCrossRefGoogle Scholar
  4. Benemann JR (1973) Nitrogen fixation in termites. Science 181:164–165PubMedCrossRefGoogle Scholar
  5. Bignell DE (2006) Termites as soil engineers and soil processors. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 183–220CrossRefGoogle Scholar
  6. Bignell DE, Eggleton P (1995) On the elevated intestinal pH of higher termites (Isoptera: Termitidae). Insect Soc 42:57–69CrossRefGoogle Scholar
  7. Bignell DE, Oskarsson H, Anderson JM (1980) Specialization of the hindgut wall for the attachment of symbiotic microorganisms in a termite Procubitermes Aburiensis. Zoomorphology 96:103–112CrossRefGoogle Scholar
  8. Boga HI, Brune A (2003) Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Appl Environ Microbiol 69:779–786PubMedCrossRefGoogle Scholar
  9. Boga HI, Ji R, Ludwig W, Brune A (2007) Sporotalea Propionica gen. nov. sp. nov., a hydrogen-oxidizing, oxygen-reducing, propionigenic firmicute from the intestinal tract of a soil-feeding termite. Arch Microbiol 187:15–27PubMedCrossRefGoogle Scholar
  10. Boga HI, Ludwig W, Brune A (2003) Sporomusa Aerivorans sp. nov., an oxygen-reducing homoacetogenic bacterium from the gut of a soil-feeding termite. Int J Syst Evol Microbiol 53:1397–1404PubMedCrossRefGoogle Scholar
  11. Brauman A, Bignell DE, Tayasu I (2000) Soil-feeding termites: biology, microbial associations and digestive mechanisms. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 233–259Google Scholar
  12. Brauman A, Kane MD, Labat M, Breznak JA (1992) Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384–1387PubMedCrossRefGoogle Scholar
  13. Brauman A, Müller JA, Garcia J-L et al (1998) Fermentative degradation of 3-hydroxybenzoate in pure culture by a novel strictly anaerobic bacterium, Sporotomaculum hydroxybenzoicum gen. nov., sp. nov. Int J Syst Bacteriol 48:215–221PubMedCrossRefGoogle Scholar
  14. Brennan Y, Callen WN, Christoffersen L et al (2004) Unusual microbial xylanases from insect guts. Appl Environ Microbiol 70:3609–3617PubMedCrossRefGoogle Scholar
  15. Breznak JA (1994) Acetogenesis from carbon dioxide in termite guts. In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York, NY, pp 303–330CrossRefGoogle Scholar
  16. 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, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 209–231Google Scholar
  17. Breznak JA, Blum JS (1991) Mixotrophy in the termite acetogen gut acetogen, Sporomusa termitida. Arch Microbiol 156:105–110CrossRefGoogle Scholar
  18. Breznak JA, Brill WJ, Mertins JW, Coppel HC (1973) Nitrogen fixation in termites. Nature 244:577–580PubMedCrossRefGoogle Scholar
  19. Breznak JA, Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39:453–487CrossRefGoogle Scholar
  20. Breznak JA, Mertins JW, Coppel HC (1974) Nitrogen fixation and methane production in a wood-eating cockroach, Cryptocercus Punctulatus Scudder (Orthoptera: Blattidae). Univ Wisc Forest Res Notes 184:1–2Google Scholar
  21. Breznak JA, Switzer JM (1986) Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl Environ Microbiol 52:623–630PubMedGoogle Scholar
  22. Brugerolle G, Radek R (2006) Symbiotic protozoa of termites. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 243–269CrossRefGoogle Scholar
  23. Brune A (1998) Termite guts: the world’s smallest bioreactors. Trends Biotechnol 16:16–21CrossRefGoogle Scholar
  24. Brune A (2006) Symbiotic associations between termites and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E et al (eds) The prokaryotes. 3rd edn, vol 1. Symbiotic associations, biotechnology, applied microbiology, Springer, New York, NY, pp 439–474CrossRefGoogle Scholar
  25. Brune A (2007) Woodworker’s digest. Nature 450:487–488PubMedCrossRefGoogle Scholar
  26. Brune A (2009a) Symbionts aiding digestion. In: Cardé RT, Resh VH (eds) Encyclopedia of insects, 2nd edn. Academic Press, New York, NY, pp 978–983CrossRefGoogle Scholar
  27. Brune A (2009b) Methanogenesis in the digestive tracts of insects. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol 1. Springer, Heidelberg, pp 707–728Google Scholar
  28. Brune A, Emerson D, Breznak JA (1995a) 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
  29. Brune A, Frenzel P, Cypionka H (2000) Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24:691–710PubMedGoogle Scholar
  30. Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3:263–269PubMedCrossRefGoogle Scholar
  31. Brune A, Kühl M (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42:1121–1127CrossRefGoogle Scholar
  32. Brune A, Miambi E, Breznak JA (1995b) Roles of oxygen and the intestinal microflora in the metabolism of lignin-derived phenylpropanoids and other monoaromatic compounds by termites. Appl Environ Microbiol 61:2688–2695PubMedGoogle Scholar
  33. Brune A, Pester M (2005) In situ measurements of metabolite fluxes: microinjection of radiotracers into insect guts and other small compartments. In: Leadbetter JR (ed) Methods in enzymology, vol 397. Elsevier, London, pp 200–212Google Scholar
  34. Brune A, Stingl U (2005) Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis. In: Overmann J (ed) Molecular basis of symbiosis. Springer, Berlin, pp 39–60Google Scholar
  35. Cleveland LR (1923) Symbiosis between termites and their intestinal protozoa. Proc Natl Acad Sci USA 9:424–428PubMedCrossRefGoogle Scholar
  36. Cornelius ML, Daigle DJ, Connick WJ Jr et al (2002) Responses of Coptotermes Formosanus and Reticulitermes Flavipes (Isoptera: Rhinotermitidae) to three types of wood rot fungi cultured on different substrates. J Econ Entomol 95:121–128PubMedCrossRefGoogle Scholar
  37. Dadd RH (1973) Insect nutrition; current developments and metabolic implications. Annu Rev Entomol 18:381–420PubMedCrossRefGoogle Scholar
  38. Dittmer NT, Suderman RJ, Jiang H et al (2004) Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca Sexta, and the malaria mosquito, Anopheles Gambiae. Insect Biochem Molec Biol 34:29–34CrossRefGoogle Scholar
  39. Donovan SE, Eggleton P, Bignell DE (2001) Gut content analysis and a new feeding group classification of termites. Ecol Entomol 26:356–366CrossRefGoogle Scholar
  40. Dröge S, Fröhlich J, Radek R, König H (2006) Spirochaeta Coccoides sp. nov., a novel coccoid spirochete from the hindgut of the termite Neotermes Castaneus. Appl Environ Microbiol 72:392–397PubMedCrossRefGoogle Scholar
  41. Dröge S, Limper U, Emtiazi F et al (2005) In vitro and in vivo sulfate reduction in the gut contents of the termite Mastotermes Darwiniensis and the rose-chafer Pachnoda Marginata. J Gen Appl Microbiol 51:57–64PubMedCrossRefGoogle Scholar
  42. Dröge S, Rachel R, Radek R, König H (2008) Treponema Isoptericolens sp. nov., a novel spirochaete from the hindgut of the termite Incisitermes Tabogae. Int J Syst Evol Microbiol 58:1079–1083PubMedCrossRefGoogle Scholar
  43. 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
  44. Eggleton P (2006) The termite gut habitat: its evolution and co-evolution. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 373–404CrossRefGoogle Scholar
  45. Eggleton P, Tayasu I (2001) Feeding groups, lifetypes and the global ecology of termites. Ecol Res 16:941–960CrossRefGoogle Scholar
  46. Eusterhues K, Rumpel C, Kleber M, Kögel-Knabner I (2003) Stabilisation of soil organic matter by interactions with minerals as revealed by mineral dissolution and oxidative degradation. Org Geochem 34:1591–1600CrossRefGoogle Scholar
  47. Fall S, Hamelin J, Ndiaye F et al (2007) Differences between bacterial communities in the gut of a soil-feeding termite (Cubitermes Niokoloensis) and its mounds. Appl Environ Microbiol 73:5199–5208PubMedCrossRefGoogle Scholar
  48. Fujita A (2004) Lysozymes in insects: what role do they play in nitrogen metabolism?. Physiol Entomol 299:305–310CrossRefGoogle Scholar
  49. Fujita A, Abe T (2002) Amino acid concentration and distribution of lysozyme and protease activities in the guts of higher termites. Physiol Entomol 27:76–78CrossRefGoogle Scholar
  50. Fujita A, Shimizu I, Abe T (2001) Distribution of lysozyme and protease, and amino acid concentration in the guts of a wood-feeding termite, ReTiculitermes Speratus (Kolbe): possible digestion of symbiont bacteria transferred by trophallaxis. Physiol Entomol 26:116–123CrossRefGoogle Scholar
  51. Geib SM, Filley TR, Hatcher PG et al (2008) Lignin degradation in wood-feeding insects. Proc Natl Acad Sci USA 105:12932–12937PubMedCrossRefGoogle Scholar
  52. Geissinger O, Herlemann DPR, Mörschel E et al (2009) The ultramicrobacterium “Elusimicrobium Minutum” gen. nov., sp. nov., the first cultivated representative of the Termite Group 1 phylum. Appl Environ Microbiol 75:2831–2840PubMedCrossRefGoogle Scholar
  53. Graber JR, Breznak JA (2004) Physiology and nutrition of Treponema primitia, an H2/CO2-acetogenic spirochete from termite hindguts. Appl Environ Microbiol 70:1307–1314PubMedCrossRefGoogle Scholar
  54. Graber JR, Breznak JA (2005) Folate cross-feeding supports symbiotic homoacetogenic spirochetes. Appl Environ Microbiol 71:1883–1889PubMedCrossRefGoogle Scholar
  55. 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 70:1315–1320PubMedCrossRefGoogle Scholar
  56. Hackstein JHP, van Alen TA, Rosenberg J (2006) Methane production by terrestrial arthropods. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 155–180CrossRefGoogle Scholar
  57. Hampl V, Silberman JD, Stechmann A et al (2008) Genetic evidence for a mitochondriate ancestry in the ‘amitochondriate’ Flagellate Trimastix pyriformis. PLoS ONE 3:e1383. doi:10.1371/journal.pone.0001383PubMedCrossRefGoogle Scholar
  58. Herlemann DPR, Geissinger O, Ikeda-Ohtsubo W et al (2009) Genomic analysis of “Elusimicrobium Minutum,” the first cultivated representative of the phylum “Elusimicrobia” (formerly Termite Group 1). Appl Environ Microbiol 75:2841–2849PubMedCrossRefGoogle Scholar
  59. Hethener P, Brauman A, Garcia JL (1992) Clostridium Termitidis sp. nov., a cellulolytic bacterium from the gut of the wood-feeding termite, Nasutitermes Lujae. Syst Appl Microbiol 15:52–58CrossRefGoogle Scholar
  60. Higashi M, Abe T, Burns TP (1992) Carbon-nitrogen balance and termite ecology. Proc R Soc Lond B 249:303–308CrossRefGoogle Scholar
  61. Hongoh Y, Deevong P, Hattori S et al (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. Appl Environ Microbiol 72:6780–6788PubMedCrossRefGoogle Scholar
  62. Hongoh Y, Deevong P, Inoue T et al (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71:6590–6599PubMedCrossRefGoogle Scholar
  63. Hongoh Y, Sharma VK, Prakash T et al (2008a) Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci USA 105:5555–5560PubMedCrossRefGoogle Scholar
  64. Hongoh Y, Sharma VK, Prakash T et al (2008b) Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322:1108–1109PubMedCrossRefGoogle Scholar
  65. Hopkins DW, Chudek JA, Bignell DE et al (1998) Application of 13C NMR to investigate the transformations and biodegradation of organic materials by wood- and soil-feeding termites, and a coprophagous litter-dwelling dipteran larva. Biodegradation 9:423–431PubMedCrossRefGoogle Scholar
  66. Hyodo F, Azuma J, Abe T (1999) Estimation of effect of passage through the gut of a lower termite, Coptotermes Formosanus Shiraki, on lignin by solid-state CP MAS C-13 NMR. Holzforschung 53:244–246CrossRefGoogle Scholar
  67. Hyodo F, Tayasu I, Inoue T et al (2003) Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Funct Ecol 17:186–193CrossRefGoogle Scholar
  68. Ikeda-Ohtsubo W, Brune A (2009) Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Mol Ecol 18:332–342PubMedCrossRefGoogle Scholar
  69. Inoue T, Kitade O, Yoshimura T, Yamaoka I (2000) Symbiotic associations with protists. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 275–288Google Scholar
  70. 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 349:67–75PubMedCrossRefGoogle Scholar
  71. Inoue T, Murashima K, Azuma J-I et al (1997) Cellulose and xylan utilization in the lower termite Reticulitermes Speratus. J Insect Physiol 43:235–242PubMedCrossRefGoogle Scholar
  72. Inoue JI, Saita K, Kudo T et al (2007) Hydrogen production by termite gut protists: characterization of iron hydrogenases of parabasalian symbionts of the termite Coptotermes Formosanus. Eukaryot Cell 6:1925–1932PubMedCrossRefGoogle Scholar
  73. Itakura S, Tanaka H, Enoki A (1999) Occurrence and metabolic role of the pyruvate dehydrogenase complex in the lower termite Coptotermes formosanus (Shiraki). Insect Biochem Molec Biol 29:625–633CrossRefGoogle Scholar
  74. Itakura S, Tanaka H, Enoki A et al (2003) Pyruvate and acetate metabolism in termite mitochondria. J Insect Physiol 49:917–926PubMedCrossRefGoogle Scholar
  75. Ji R, Brune A (2001) Transformation and mineralization of 14C-labeled cellulose, peptidoglycan, and protein by the soil-feeding termite Cubitermes Orthognathus. Biol Fertil Soils 33:166–174CrossRefGoogle Scholar
  76. Ji R, Brune A (2005) Digestion of peptidic residues in humic substances by an alkali-stable and humic-acid-tolerant proteolytic activity in the gut of soil-feeding termites. Soil Biol Biochem 37:1648–1655CrossRefGoogle Scholar
  77. Ji R, Brune A (2006) Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry 78:267–283CrossRefGoogle Scholar
  78. Ji R, Kappler A, Brune A (2000) Transformation and mineralization of synthetic 14C-labeled humic model compounds by soil-feeding termites. Soil Biol Biochem 32:1281–1291CrossRefGoogle Scholar
  79. Johjima T, Taprab Y, Noparatnaraporn N et al (2006) Large-scale identification of transcripts expressed in a symbiotic fungus (Termitomyces) during plant biomass degradation. Appl Microbiol Biotechnol 73:195–203PubMedCrossRefGoogle Scholar
  80. Kappler A, Brune 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. Appl Soil Ecol 13:219–229CrossRefGoogle Scholar
  81. Kappler A, Brune A (2002) Dynamics of redox potential and changes in redox state of iron and humic acids during gut passage in soil-feeding termites (Cubitermes spp). Soil Biol Biochem 34:221–227CrossRefGoogle Scholar
  82. Katsumata KS, Jin Z, Hori K, Iiyama K (2007) Structural changes in lignin of tropical woods during digestion by termite, Cryptotermes Brevis. J Wood Sci 53:419–426CrossRefGoogle Scholar
  83. Kiuchi I, Moriya S, Kudo T (2004) Two different size-distributions of engulfment-related vesicles among symbiotic protists of the lower termites, Reticulitermes Speratus. Microb Environ 19:211–214CrossRefGoogle Scholar
  84. Kuhnigk T, Borst E-M, Ritter A et al (1994) Degradation of lignin monomers by the hindgut flora of xylophagous termites. System Appl Microbiol 17:76–85CrossRefGoogle Scholar
  85. Kuhnigk T, Branke J, Krekeler D et al (1996) A feasible role of sulfate-reducing bacteria in the termite gut. System Appl Microbiol 19:139–149CrossRefGoogle Scholar
  86. Kuhnigk T, König H (1997) Degradation of dimeric lignin model compounds by aerobic bacteria isolated from the hindgut of xylophagous termites. J Basic Microbiol 37:205–211PubMedCrossRefGoogle Scholar
  87. Köhler T, Stingl U, Meuser K, Brune A (2008) Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp). Environ Microbiol 10:1260–1270PubMedCrossRefGoogle Scholar
  88. König H, Fröhlich J, Hertel H (2006) Diversity and lignocellulolytic activities of cultured microorgansims. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 271–301CrossRefGoogle Scholar
  89. 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
  90. Leadbetter JR, Crosby LD, Breznak JA (1998) Methanobrevibacter Filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch Microbiol 169:287–292PubMedCrossRefGoogle Scholar
  91. Leadbetter JR, Schmidt TM, Graber JR, Breznak JA (1999) Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283:686–689PubMedCrossRefGoogle Scholar
  92. Lemke T, Stingl U, Egert M et al (2003) Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda Ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microbiol 69:6650–6658PubMedCrossRefGoogle Scholar
  93. Lemke T, van Alen T, Hackstein JHP, Brune A (2001) Cross-epithelial hydrogen transfer from the midgut compartment drives methanogenesis in the hindgut of cockroaches. Appl Environ Microbiol 67:4657–4661PubMedCrossRefGoogle Scholar
  94. Li L, Fröhlich J, König H (2006) Cellulose digestion in the termite gut. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 221–241CrossRefGoogle Scholar
  95. Li L, Fröhlich J, Pfeiffer P, König H (2003) Termite gut symbiotic Archaezoa are becoming living metabolic fossils. Eukaryot Cell 2:1091–1098PubMedCrossRefGoogle Scholar
  96. Lighton JRB, Ottesen EA (2005) To DGC or not to DGC: oxygen guarding in the termite Zootermopsis Nevadensis (Isoptera: Termopsidae). J Exp Biol 208:4671–4678PubMedCrossRefGoogle Scholar
  97. Lilburn TG, Kim KS, Ostrom NE et al (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498PubMedCrossRefGoogle Scholar
  98. Lloyd D (2004) ‘Anaerobic protists’: some misconceptions and confusions. Microbiology 150:1115–1116PubMedCrossRefGoogle Scholar
  99. Machida M, Kitade O, Miura T, Matsumoto T (2001) Nitrogen recycling through proctodeal trophallaxis in the Japanese damp-wood termite Hodotermopsis japonica (Isoptera, Termopsidae). Insect Soc 48:52–56CrossRefGoogle Scholar
  100. Messer AC, Lee MJ (1989) Effect of chemical treatments on methane emission by the hindgut microbiota in the termite Zootermopsis Angusticollis. Microb Ecol 18:275–284CrossRefGoogle Scholar
  101. Minkley N, Fujita A, Brune A, Kirchner WH (2006) Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insect Soc 53:339–344CrossRefGoogle Scholar
  102. Müller M (1988) Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol 42:465–488PubMedCrossRefGoogle Scholar
  103. Nakashima K, Watanabe H, Saitoh H (2002) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes Formosanus Shiraki. Insect Biochem Molec Biol 32:777–784CrossRefGoogle Scholar
  104. Ndiaye D, Lensi R, Lepage M, Brauman A (2004) The effect of the soil-feeding termite Cubitermes Niokoloensis on soil microbial activity in a semi-arid savanna in West Africa. Plant Soil 259:277–286CrossRefGoogle Scholar
  105. Ngugi DK, Ji R, Brune A (2010) Nitrogen mineralization, denitrification, and nitrate ammonification by soil-feeding termites – a 15 N-based approach. Biogeochemistry (DOI:10.1007/s10533-010-9478-6)Google Scholar
  106. Ngugi DK, Tsanuo MK, Boga HI (2007) Benzoic acid-degrading bacteria from the intestinal tract of Macrotermes michaelseni Sjostedt. J Basic Microbiol 47:87–92CrossRefGoogle Scholar
  107. Noda S, Kitade O, Inoue T et al (2007) Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol Ecol 16:1257–1266PubMedCrossRefGoogle Scholar
  108. Noda S, Ohkuma M, Kudo T (2002) Nitrogen fixation genes expressed in the symbiotic microbial community in the gut of the termite Coptotermes Formosanus. Microbes Environ 17:139–143CrossRefGoogle Scholar
  109. Noda S, Ohkuma M, Usami R et al (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
  110. Noirot C (1992) From wood- to humus-feeding: an important trend in termite evolution. In: Billen J (eds) Biology and evolution of social insects. Leuven University Press, Leuven, Belgium, pp 107–119Google Scholar
  111. Odelson DA, Breznak JA (1983) Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol 45:1602–1613PubMedGoogle Scholar
  112. Odelson DA, Breznak JA (1985a) Nutrition and growth characteristics of Trichomitopsis Termopsidis, a cellulolytic protozoan from termites. Appl Environ Microbiol 49:614–621PubMedGoogle Scholar
  113. Odelson DA, Breznak JA (1985b) Cellulase and other polymer-hydrolyzing activities of Trichomitopsis Termopsidis, a symbiotic protozoan from termites. Appl Environ Microbiol 49:622–626PubMedGoogle Scholar
  114. Ohkuma M (2002) Symbiosis in the termite gut: culture-independent molecular approaches. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic Publishers, Dordrecht, pp 717–730Google Scholar
  115. Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61:1–9PubMedGoogle Scholar
  116. Ohkuma M (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16:345–352PubMedCrossRefGoogle Scholar
  117. 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
  118. Ohkuma M, Noda S, Usami R et al (1996) Diversity of nitrogen-fixation genes in the symbiotic intestinal microflora of the termite ReticuLitermes Speratus. Appl Environ Microbiol 62:2747–2752PubMedGoogle Scholar
  119. Ohtoko K, Ohkuma M, Moriya S et al (2000) Diverse genes of cellulase homologues of glycosyl hydrolase family 45 from the symbiotic protists in the hindgut of the termite Reticulitermes Speratus. Extremophiles 4:343–349PubMedCrossRefGoogle Scholar
  120. Olson JW, Maier RJ (2002) Molecular hydrogen as an energy source for Helicobacter pylori. Science 298:1788–1790PubMedCrossRefGoogle Scholar
  121. Ottesen EA, Hong JW, Quake SR, Leadbetter JR (2006) Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 314:1464–1467PubMedCrossRefGoogle Scholar
  122. 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 8:1261–1270PubMedCrossRefGoogle Scholar
  123. Pester M, Brune A (2007) Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J 1:551–565PubMedCrossRefGoogle Scholar
  124. Pester M, Tholen A, Friedrich MW, Brune A (2007) Methane oxidation in termite hindguts: absence of evidence and evidence of absence. Appl Environ Microbiol 73:2024–2028PubMedCrossRefGoogle Scholar
  125. Potrikus CJ, Breznak JA (1981) Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. Proc Natl Acad Sci USA 78:4601–4605PubMedCrossRefGoogle Scholar
  126. Rasmussen RA, Khalil MAK (1983) Global production of methane by termites. Nature 301:700–702CrossRefGoogle Scholar
  127. Rouland-Lefèvre C (2000) Symbiosis with fungi. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 289–306Google Scholar
  128. Rouland-Lefèvre C, Inoue T, Johjima T (2006) Termitomyces/termite interactions. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 335–350CrossRefGoogle Scholar
  129. Sabree ZL, Kambhampati S, Moran NA (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci USA 106:19521–19526PubMedCrossRefGoogle Scholar
  130. Salmassi TM, Leadbetter JR (2003) Molecular aspects of CO2-reductive acetogenesis in cultivated spirochetes and the gut community of the termite Zootermopsis Angusticollis. Microbiology 149:2529–2537PubMedCrossRefGoogle Scholar
  131. Sato T, Hongoh Y, Noda S et al (2008) Candidatus Desulfovibrio Trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha Agilis in termite gut. Environ Microbiol 11:1007–1015PubMedCrossRefGoogle Scholar
  132. Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280PubMedGoogle Scholar
  133. Schmitt-Wagner D, Brune A (1999) Hydrogen profiles and localization of methanogenic activities in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp). Appl Environ Microbiol 65:4490–4496PubMedGoogle Scholar
  134. Schmitt-Wagner D, Friedrich MW, Wagner B, Brune A (2003a) Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp). Appl Environ Microbiol 69:6007–6017PubMedCrossRefGoogle Scholar
  135. Schmitt-Wagner D, Friedrich MW, Wagner B, Brune A (2003b) Axial dynamics, stability, and interspecies similarity of bacterial community structure in the highly compartmentalized gut of soil-feeding termites (Cubitermes spp). Appl Environ Microbiol 69:6018–6024PubMedCrossRefGoogle Scholar
  136. Schramm A (2006) Microsensors for the study of microenvironments and processes in the intestine of invertebrates. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 463–473CrossRefGoogle Scholar
  137. Schultz JE, Breznak JA (1978) Heterotrophic bacteria present in hindguts of wood-eating termites [Reticulitermes Flavipes] (Kollar). Appl Environ Microbiol 35:930–936PubMedGoogle Scholar
  138. Schultz JE, Breznak JA (1979) Cross-feeding of lactate between Streptococcus Lactis and Bacteroides sp. isolated from termite hindguts. Appl Environ Microbiol 37:1206–1210PubMedGoogle Scholar
  139. Slaytor M (1992) Cellulose digestion in termites and cockroaches: what role do symbionts play?. Comp Biochem Physiol 103B:775–784Google Scholar
  140. Slaytor M (2000) Energy metabolism in the termite gut and its gut microbiota. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 307–332Google Scholar
  141. Slaytor M, Chappell DJ (1994) Nitrogen metabolism in termites. Comp Biochem Physiol 107B:1–10Google Scholar
  142. Sugimoto A, Bignell DE, MacDonald JA (2000) Global impact of termites on the carbon cycle and atmospheric trace gases. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 409–435Google Scholar
  143. Sugimoto A, Inoue T, Tayasu I et al (1998) Methane and hydrogen production in a termite-symbiont system. Ecol Res 13:241–257CrossRefGoogle Scholar
  144. Tanaka H, Aoyagi H, Shina S et al (2006) Influence of the diet components on the symbiotic microorganisms community in hindgut of Coptotermes formosanus Shiraki. Appl Microbiol Biotechnol 71:907–917PubMedCrossRefGoogle Scholar
  145. Taprab Y, Johjima T, Maeda Y et al (2005) Symbiotic fungi produce laccases potentially involved in phenol degradation in fungus combs of fungus-growing termites in Thailand. Appl Environ Microbiol 71:7696–7704PubMedCrossRefGoogle Scholar
  146. Tartar A, Wheeler MM, Zhou X et al (2009) Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnol Biofuels 2:25PubMedCrossRefGoogle Scholar
  147. Tayasu I (1998) The use of carbon and nitrogen isotope ratios in termite research. Ecol Res 13:377–387CrossRefGoogle Scholar
  148. Tholen A, Brune A (1999) Localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp). Appl Environ Microbiol 65:4497–4505PubMedGoogle Scholar
  149. 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. Environ Microbiol 2:436–449PubMedCrossRefGoogle Scholar
  150. Tholen A, Pester M, Brune A (2007) Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter Cuticularis at low oxygen fluxes. FEMS Microbiol Ecol 62:303–312PubMedCrossRefGoogle Scholar
  151. Tholen A, Schink B, Brune A (1997) The gut microflora of Reticulitermes Flavipes, its relation to oxygen, and evidence for oxygen-dependent acetogenesis by the most abundant Enterococcus sp. FEMS Microbiol Ecol 24:137–149CrossRefGoogle Scholar
  152. Thongaram T, Hongoh Y, Kosono S et al (2005) Comparison of bacterial communities in the alkaline gut segment among various species of higher termites. Extremophiles 9:229–238PubMedCrossRefGoogle Scholar
  153. Todaka N, Inoue T, Saita K et al (2010a) Phylogenetic analysis of cellulolytic enzyme genes from representative lineages of termites and a related cockroach. PLoS ONE 5:e8636PubMedCrossRefGoogle Scholar
  154. Todaka N, Lopez CM, Inoue T et al (2010b) Heterologous expression and characterization of an endoglucanase from a symbiotic protist of the lower termite, Reticulitermes speratus. Appl Microbiol Biotechnol 160:1168–1178Google Scholar
  155. Todaka N, Moriya S, Saita K et al (2007) Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes Speratus. FEMS Microbiol Ecol 59:592–599PubMedCrossRefGoogle Scholar
  156. Tokuda G, Lo N, Watanabe H et al (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol Ecol 13:3219–3228PubMedCrossRefGoogle Scholar
  157. Tokuda G, Lo N, Watanabe H (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
  158. Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339PubMedCrossRefGoogle Scholar
  159. Tokuda G, Watanabe H, Lo N (2007) Does correlation of cellulase gene expression and cellulolytic activity in the gut of termite suggest synergistic collaboration of cellulases? Gene 401:131–134PubMedCrossRefGoogle Scholar
  160. Vairavamurthy A, Wang S (2002) Organic nitrogen in geomacromolecules: insights on speciation and transformation with K-edge XANES spectroscopy. Environ Sci Technol 36:3050–3056PubMedCrossRefGoogle Scholar
  161. Vu AT, Nguyen NC, Leadbetter JR (2004) Iron reduction in the metal-rich guts of wood-feeding termites. Geobiology 2:239–247CrossRefGoogle Scholar
  162. Warnecke F, Luginbühl P, Ivanova N et al (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedCrossRefGoogle Scholar
  163. 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 59:1983–1992PubMedCrossRefGoogle Scholar
  164. Watanabe H, Takase A, Tokuda G et al (2006) Symbiotic “Archaezoa” of the primitive termite Mastotermes darwiniensis still play a role in cellulase production. Eukaryot Cell 5:1571–1576PubMedCrossRefGoogle Scholar
  165. Watanabe H, Tokuda G (2009) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632CrossRefGoogle Scholar
  166. Wertz JT, Breznak JA (2007a) Stenoxybacter Acetivorans gen. nov., sp. nov., an acetate-oxidizing obligate microaerophile among diverse O2-consuming bacteria from termite guts. Appl Environ Microbiol 73:6819–6828PubMedCrossRefGoogle Scholar
  167. Wertz JT, Breznak JA (2007b) Physiological ecology of Stenoxybacter Acetivorans, an obligate microaerophile in termite guts. Appl Environ Microbiol 73:6829–6841PubMedCrossRefGoogle Scholar
  168. Yamada A, Inoue T, Noda Y et al (2007) Evolutionary trend of phylogenetic diversity of nitrogen fixation genes in the gut community of wood-feeding termites. Mol Ecol 16:3768–3777PubMedCrossRefGoogle Scholar
  169. Yamin MA (1978) Axenic cultivation of the cellulolytic flagellate Trichomitopsis termopsidis (Cleveland) from the termite Zootermopsis. J Protozool 25:535–538Google Scholar
  170. Yamin MA (1981) Cellulose metabolism by the flagellate Trichonympha from a termite is independent of endosymbiotic bacteria. Science 211:58–59PubMedCrossRefGoogle Scholar
  171. Yamin MA, Trager W (1979) Cellulolytic activity of an axenically-cultivated termite flagellate, Trichomitopsis Termopsidis. J Gen Microbiol 113:417–420Google Scholar
  172. 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
  173. Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554PubMedCrossRefGoogle Scholar
  174. Zhou X, Smith JA, Oi FM et al (2007) Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes Flavipes. Gene 395:29–39PubMedCrossRefGoogle Scholar
  175. Zimmerman PR, Greenberg JP, Wandiga SO, Crutzen PJ (1982) Termites: A potentially large source of atmospheric methane, carbon dioxide, and molecular hydrogen. Science 218:563–565PubMedCrossRefGoogle Scholar

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© Springer Netherlands 2010

Authors and Affiliations

  1. 1.Department of BiogeochemistryMax Planck Institute for Terrestrial MicrobiologyMarburgGermany
  2. 2.Microbe Division(Japan Collection of Microorganisms), RIKEN Bioresource CenterSaitamaJapan

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