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Role of the Termite Gut Microbiota in Symbiotic Digestion

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Biology of Termites: a Modern Synthesis

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.

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References

  • 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 73:710–718

    Article  PubMed  CAS  Google Scholar 

  • Azuma J, Nishimoto K, Koshijima T (1984) Studies on digestive system of termites. II. Properties of carbohydrolases of termite Coptotermes formosanus Shiraki. Wood Res 70:1–16

    CAS  Google Scholar 

  • 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 173:126–173

    Article  PubMed  CAS  Google Scholar 

  • Benemann JR (1973) Nitrogen fixation in termites. Science 181:164–165

    Article  PubMed  CAS  Google Scholar 

  • 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 183–220

    Chapter  Google Scholar 

  • Bignell DE, Eggleton P (1995) On the elevated intestinal pH of higher termites (Isoptera: Termitidae). Insect Soc 42:57–69

    Article  Google Scholar 

  • Bignell DE, Oskarsson H, Anderson JM (1980) Specialization of the hindgut wall for the attachment of symbiotic microorganisms in a termite Procubitermes Aburiensis. Zoomorphology 96:103–112

    Article  Google Scholar 

  • Boga HI, Brune A (2003) Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Appl Environ Microbiol 69:779–786

    Article  PubMed  CAS  Google Scholar 

  • 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 187:15–27

    Article  PubMed  CAS  Google Scholar 

  • 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 53:1397–1404

    Article  PubMed  CAS  Google Scholar 

  • 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 233–259

    Google Scholar 

  • Brauman A, Kane MD, Labat M, Breznak JA (1992) Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384–1387

    Article  PubMed  CAS  Google Scholar 

  • 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 48:215–221

    Article  PubMed  CAS  Google Scholar 

  • Brennan Y, Callen WN, Christoffersen L et al (2004) Unusual microbial xylanases from insect guts. Appl Environ Microbiol 70:3609–3617

    Article  PubMed  CAS  Google Scholar 

  • Breznak JA (1994) Acetogenesis from carbon dioxide in termite guts. In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York, NY, pp 303–330

    Chapter  Google Scholar 

  • 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 209–231

    Google Scholar 

  • Breznak JA, Blum JS (1991) Mixotrophy in the termite acetogen gut acetogen, Sporomusa termitida. Arch Microbiol 156:105–110

    Article  CAS  Google Scholar 

  • Breznak JA, Brill WJ, Mertins JW, Coppel HC (1973) Nitrogen fixation in termites. Nature 244:577–580

    Article  PubMed  CAS  Google Scholar 

  • Breznak JA, Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39:453–487

    Article  CAS  Google Scholar 

  • 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 184:1–2

    Google Scholar 

  • Breznak JA, Switzer JM (1986) Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl Environ Microbiol 52:623–630

    PubMed  CAS  Google Scholar 

  • 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 243–269

    Chapter  Google Scholar 

  • Brune A (1998) Termite guts: the world’s smallest bioreactors. Trends Biotechnol 16:16–21

    Article  CAS  Google Scholar 

  • 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 439–474

    Chapter  Google Scholar 

  • Brune A (2007) Woodworker’s digest. Nature 450:487–488

    Article  PubMed  CAS  Google Scholar 

  • Brune A (2009a) Symbionts aiding digestion. In: Cardé RT, Resh VH (eds) Encyclopedia of insects, 2nd edn. Academic Press, New York, NY, pp 978–983

    Chapter  Google Scholar 

  • 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 707–728

    Google Scholar 

  • 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 61:2681–2687

    PubMed  CAS  Google Scholar 

  • Brune A, Frenzel P, Cypionka H (2000) Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24:691–710

    PubMed  CAS  Google Scholar 

  • Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3:263–269

    Article  PubMed  CAS  Google Scholar 

  • Brune A, Kühl M (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42:1121–1127

    Article  CAS  Google Scholar 

  • 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 61:2688–2695

    PubMed  CAS  Google Scholar 

  • 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 200–212

    Google Scholar 

  • 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 39–60

    Google Scholar 

  • Cleveland LR (1923) Symbiosis between termites and their intestinal protozoa. Proc Natl Acad Sci USA 9:424–428

    Article  PubMed  CAS  Google Scholar 

  • 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 95:121–128

    Article  PubMed  Google Scholar 

  • Dadd RH (1973) Insect nutrition; current developments and metabolic implications. Annu Rev Entomol 18:381–420

    Article  PubMed  CAS  Google Scholar 

  • 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 34:29–34

    Article  CAS  Google Scholar 

  • Donovan SE, Eggleton P, Bignell DE (2001) Gut content analysis and a new feeding group classification of termites. Ecol Entomol 26:356–366

    Article  Google Scholar 

  • 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 72:392–397

    Article  PubMed  CAS  Google Scholar 

  • 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 51:57–64

    Article  PubMed  Google Scholar 

  • 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 58:1079–1083

    Article  PubMed  CAS  Google Scholar 

  • 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 63:4039–4046

    PubMed  CAS  Google Scholar 

  • 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 373–404

    Chapter  Google Scholar 

  • Eggleton P, Tayasu I (2001) Feeding groups, lifetypes and the global ecology of termites. Ecol Res 16:941–960

    Article  Google Scholar 

  • 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 34:1591–1600

    Article  CAS  Google Scholar 

  • 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 73:5199–5208

    Article  PubMed  CAS  Google Scholar 

  • Fujita A (2004) Lysozymes in insects: what role do they play in nitrogen metabolism?. Physiol Entomol 299:305–310

    Article  Google Scholar 

  • Fujita A, Abe T (2002) Amino acid concentration and distribution of lysozyme and protease activities in the guts of higher termites. Physiol Entomol 27:76–78

    Article  CAS  Google Scholar 

  • 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 26:116–123

    Article  CAS  Google Scholar 

  • Geib SM, Filley TR, Hatcher PG et al (2008) Lignin degradation in wood-feeding insects. Proc Natl Acad Sci USA 105:12932–12937

    Article  PubMed  CAS  Google Scholar 

  • 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 75:2831–2840

    Article  PubMed  CAS  Google Scholar 

  • Graber JR, Breznak JA (2004) Physiology and nutrition of Treponema primitia, an H2/CO2-acetogenic spirochete from termite hindguts. Appl Environ Microbiol 70:1307–1314

    Article  PubMed  CAS  Google Scholar 

  • Graber JR, Breznak JA (2005) Folate cross-feeding supports symbiotic homoacetogenic spirochetes. Appl Environ Microbiol 71:1883–1889

    Article  PubMed  CAS  Google Scholar 

  • 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 70:1315–1320

    Article  PubMed  CAS  Google Scholar 

  • 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 155–180

    Chapter  Google Scholar 

  • 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.0001383

    Article  PubMed  CAS  Google Scholar 

  • 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 75:2841–2849

    Article  PubMed  CAS  Google Scholar 

  • 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 15:52–58

    Article  CAS  Google Scholar 

  • Higashi M, Abe T, Burns TP (1992) Carbon-nitrogen balance and termite ecology. Proc R Soc Lond B 249:303–308

    Article  Google Scholar 

  • 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 72:6780–6788

    Article  PubMed  CAS  Google Scholar 

  • 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 71:6590–6599

    Article  PubMed  CAS  Google Scholar 

  • 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 105:5555–5560

    Article  PubMed  CAS  Google Scholar 

  • 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 322:1108–1109

    Article  PubMed  CAS  Google Scholar 

  • 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 9:423–431

    Article  PubMed  CAS  Google Scholar 

  • 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 53:244–246

    Article  CAS  Google Scholar 

  • 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 17:186–193

    Article  Google Scholar 

  • Ikeda-Ohtsubo W, Brune A (2009) Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Mol Ecol 18:332–342

    Article  PubMed  CAS  Google Scholar 

  • 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 275–288

    Google Scholar 

  • 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 349:67–75

    Article  PubMed  CAS  Google Scholar 

  • Inoue T, Murashima K, Azuma J-I et al (1997) Cellulose and xylan utilization in the lower termite Reticulitermes Speratus. J Insect Physiol 43:235–242

    Article  PubMed  CAS  Google Scholar 

  • 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 6:1925–1932

    Article  PubMed  CAS  Google Scholar 

  • 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 29:625–633

    Article  CAS  Google Scholar 

  • Itakura S, Tanaka H, Enoki A et al (2003) Pyruvate and acetate metabolism in termite mitochondria. J Insect Physiol 49:917–926

    Article  PubMed  CAS  Google Scholar 

  • 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 33:166–174

    Article  CAS  Google Scholar 

  • 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 37:1648–1655

    Article  CAS  Google Scholar 

  • Ji R, Brune A (2006) Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry 78:267–283

    Article  CAS  Google Scholar 

  • Ji R, Kappler A, Brune A (2000) Transformation and mineralization of synthetic 14C-labeled humic model compounds by soil-feeding termites. Soil Biol Biochem 32:1281–1291

    Article  CAS  Google Scholar 

  • 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 73:195–203

    Article  PubMed  CAS  Google Scholar 

  • 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 13:219–229

    Article  Google Scholar 

  • 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 34:221–227

    Article  CAS  Google Scholar 

  • 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 53:419–426

    Article  CAS  Google Scholar 

  • 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 19:211–214

    Article  Google Scholar 

  • Kuhnigk T, Borst E-M, Ritter A et al (1994) Degradation of lignin monomers by the hindgut flora of xylophagous termites. System Appl Microbiol 17:76–85

    Article  CAS  Google Scholar 

  • Kuhnigk T, Branke J, Krekeler D et al (1996) A feasible role of sulfate-reducing bacteria in the termite gut. System Appl Microbiol 19:139–149

    Article  CAS  Google Scholar 

  • Kuhnigk T, König H (1997) Degradation of dimeric lignin model compounds by aerobic bacteria isolated from the hindgut of xylophagous termites. J Basic Microbiol 37:205–211

    Article  PubMed  CAS  Google Scholar 

  • 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 10:1260–1270

    Article  PubMed  CAS  Google Scholar 

  • 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 271–301

    Chapter  Google Scholar 

  • 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 62:3620–3631

    PubMed  CAS  Google Scholar 

  • Leadbetter JR, Crosby LD, Breznak JA (1998) Methanobrevibacter Filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch Microbiol 169:287–292

    Article  PubMed  CAS  Google Scholar 

  • Leadbetter JR, Schmidt TM, Graber JR, Breznak JA (1999) Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283:686–689

    Article  PubMed  CAS  Google Scholar 

  • 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 69:6650–6658

    Article  PubMed  CAS  Google Scholar 

  • 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 67:4657–4661

    Article  PubMed  CAS  Google Scholar 

  • 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 221–241

    Chapter  Google Scholar 

  • Li L, Fröhlich J, Pfeiffer P, König H (2003) Termite gut symbiotic Archaezoa are becoming living metabolic fossils. Eukaryot Cell 2:1091–1098

    Article  PubMed  CAS  Google Scholar 

  • Lighton JRB, Ottesen EA (2005) To DGC or not to DGC: oxygen guarding in the termite Zootermopsis Nevadensis (Isoptera: Termopsidae). J Exp Biol 208:4671–4678

    Article  PubMed  CAS  Google Scholar 

  • Lilburn TG, Kim KS, Ostrom NE et al (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498

    Article  PubMed  CAS  Google Scholar 

  • Lloyd D (2004) ‘Anaerobic protists’: some misconceptions and confusions. Microbiology 150:1115–1116

    Article  PubMed  CAS  Google Scholar 

  • 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 48:52–56

    Article  Google Scholar 

  • Messer AC, Lee MJ (1989) Effect of chemical treatments on methane emission by the hindgut microbiota in the termite Zootermopsis Angusticollis. Microb Ecol 18:275–284

    Article  CAS  Google Scholar 

  • Minkley N, Fujita A, Brune A, Kirchner WH (2006) Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insect Soc 53:339–344

    Article  Google Scholar 

  • Müller M (1988) Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol 42:465–488

    Article  PubMed  Google Scholar 

  • Nakashima K, Watanabe H, Saitoh H (2002) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes Formosanus Shiraki. Insect Biochem Molec Biol 32:777–784

    Article  CAS  Google Scholar 

  • 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 259:277–286

    Article  CAS  Google Scholar 

  • 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 

  • Ngugi DK, Tsanuo MK, Boga HI (2007) Benzoic acid-degrading bacteria from the intestinal tract of Macrotermes michaelseni Sjostedt. J Basic Microbiol 47:87–92

    Article  CAS  Google Scholar 

  • 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 16:1257–1266

    Article  PubMed  CAS  Google Scholar 

  • 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 17:139–143

    Article  Google Scholar 

  • 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 65:4935–4942

    PubMed  CAS  Google Scholar 

  • 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 107–119

    Google Scholar 

  • Odelson DA, Breznak JA (1983) Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol 45:1602–1613

    PubMed  CAS  Google Scholar 

  • Odelson DA, Breznak JA (1985a) Nutrition and growth characteristics of Trichomitopsis Termopsidis, a cellulolytic protozoan from termites. Appl Environ Microbiol 49:614–621

    PubMed  CAS  Google Scholar 

  • Odelson DA, Breznak JA (1985b) Cellulase and other polymer-hydrolyzing activities of Trichomitopsis Termopsidis, a symbiotic protozoan from termites. Appl Environ Microbiol 49:622–626

    PubMed  CAS  Google Scholar 

  • 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 717–730

    Google Scholar 

  • Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61:1–9

    PubMed  CAS  Google Scholar 

  • Ohkuma M (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16:345–352

    Article  PubMed  CAS  Google Scholar 

  • 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 65:4926–4934

    PubMed  CAS  Google Scholar 

  • 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 62:2747–2752

    PubMed  CAS  Google Scholar 

  • 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 4:343–349

    Article  PubMed  CAS  Google Scholar 

  • Olson JW, Maier RJ (2002) Molecular hydrogen as an energy source for Helicobacter pylori. Science 298:1788–1790

    Article  PubMed  CAS  Google Scholar 

  • Ottesen EA, Hong JW, Quake SR, Leadbetter JR (2006) Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 314:1464–1467

    Article  PubMed  CAS  Google Scholar 

  • 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 8:1261–1270

    Article  PubMed  CAS  Google Scholar 

  • Pester M, Brune A (2007) Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J 1:551–565

    Article  PubMed  CAS  Google Scholar 

  • Pester M, Tholen A, Friedrich MW, Brune A (2007) Methane oxidation in termite hindguts: absence of evidence and evidence of absence. Appl Environ Microbiol 73:2024–2028

    Article  PubMed  CAS  Google Scholar 

  • Potrikus CJ, Breznak JA (1981) Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. Proc Natl Acad Sci USA 78:4601–4605

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen RA, Khalil MAK (1983) Global production of methane by termites. Nature 301:700–702

    Article  CAS  Google Scholar 

  • 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 289–306

    Google Scholar 

  • 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 335–350

    Chapter  Google Scholar 

  • Sabree ZL, Kambhampati S, Moran NA (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci USA 106:19521–19526

    Article  PubMed  CAS  Google Scholar 

  • Salmassi TM, Leadbetter JR (2003) Molecular aspects of CO2-reductive acetogenesis in cultivated spirochetes and the gut community of the termite Zootermopsis Angusticollis. Microbiology 149:2529–2537

    Article  PubMed  CAS  Google Scholar 

  • 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 11:1007–1015

    Article  PubMed  Google Scholar 

  • Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280

    PubMed  CAS  Google Scholar 

  • 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 65:4490–4496

    PubMed  CAS  Google Scholar 

  • 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 69:6007–6017

    Article  PubMed  CAS  Google Scholar 

  • 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 69:6018–6024

    Article  PubMed  CAS  Google Scholar 

  • 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 463–473

    Chapter  Google Scholar 

  • Schultz JE, Breznak JA (1978) Heterotrophic bacteria present in hindguts of wood-eating termites [Reticulitermes Flavipes] (Kollar). Appl Environ Microbiol 35:930–936

    PubMed  CAS  Google Scholar 

  • Schultz JE, Breznak JA (1979) Cross-feeding of lactate between Streptococcus Lactis and Bacteroides sp. isolated from termite hindguts. Appl Environ Microbiol 37:1206–1210

    PubMed  CAS  Google Scholar 

  • Slaytor M (1992) Cellulose digestion in termites and cockroaches: what role do symbionts play?. Comp Biochem Physiol 103B:775–784

    CAS  Google Scholar 

  • 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 307–332

    Google Scholar 

  • Slaytor M, Chappell DJ (1994) Nitrogen metabolism in termites. Comp Biochem Physiol 107B:1–10

    CAS  Google Scholar 

  • 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 409–435

    Google Scholar 

  • Sugimoto A, Inoue T, Tayasu I et al (1998) Methane and hydrogen production in a termite-symbiont system. Ecol Res 13:241–257

    Article  CAS  Google Scholar 

  • 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 71:907–917

    Article  PubMed  CAS  Google Scholar 

  • 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 71:7696–7704

    Article  PubMed  CAS  Google Scholar 

  • 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 2:25

    Article  PubMed  CAS  Google Scholar 

  • Tayasu I (1998) The use of carbon and nitrogen isotope ratios in termite research. Ecol Res 13:377–387

    Article  Google Scholar 

  • 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 65:4497–4505

    PubMed  CAS  Google Scholar 

  • 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 2:436–449

    Article  PubMed  CAS  Google Scholar 

  • Tholen A, Pester M, Brune A (2007) Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter Cuticularis at low oxygen fluxes. FEMS Microbiol Ecol 62:303–312

    Article  PubMed  CAS  Google Scholar 

  • 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 24:137–149

    Article  CAS  Google Scholar 

  • 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 9:229–238

    Article  PubMed  Google Scholar 

  • 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:e8636

    Article  PubMed  CAS  Google Scholar 

  • 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 160:1168–1178

    CAS  Google Scholar 

  • 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 59:592–599

    Article  PubMed  CAS  Google Scholar 

  • 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 13:3219–3228

    Article  PubMed  CAS  Google Scholar 

  • 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 30:372–380

    CAS  Google Scholar 

  • Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339

    Article  PubMed  CAS  Google Scholar 

  • 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 401:131–134

    Article  PubMed  CAS  Google Scholar 

  • Vairavamurthy A, Wang S (2002) Organic nitrogen in geomacromolecules: insights on speciation and transformation with K-edge XANES spectroscopy. Environ Sci Technol 36:3050–3056

    Article  PubMed  CAS  Google Scholar 

  • Vu AT, Nguyen NC, Leadbetter JR (2004) Iron reduction in the metal-rich guts of wood-feeding termites. Geobiology 2:239–247

    Article  CAS  Google Scholar 

  • Warnecke F, Luginbühl P, Ivanova N et al (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565

    Article  PubMed  CAS  Google Scholar 

  • 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 59:1983–1992

    Article  PubMed  CAS  Google Scholar 

  • 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 5:1571–1576

    Article  PubMed  CAS  Google Scholar 

  • Watanabe H, Tokuda G (2009) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632

    Article  CAS  Google Scholar 

  • 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 73:6819–6828

    Article  PubMed  CAS  Google Scholar 

  • Wertz JT, Breznak JA (2007b) Physiological ecology of Stenoxybacter Acetivorans, an obligate microaerophile in termite guts. Appl Environ Microbiol 73:6829–6841

    Article  PubMed  CAS  Google Scholar 

  • 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 16:3768–3777

    Article  PubMed  CAS  Google Scholar 

  • Yamin MA (1978) Axenic cultivation of the cellulolytic flagellate Trichomitopsis termopsidis (Cleveland) from the termite Zootermopsis. J Protozool 25:535–538

    Google Scholar 

  • Yamin MA (1981) Cellulose metabolism by the flagellate Trichonympha from a termite is independent of endosymbiotic bacteria. Science 211:58–59

    Article  PubMed  CAS  Google Scholar 

  • Yamin MA, Trager W (1979) Cellulolytic activity of an axenically-cultivated termite flagellate, Trichomitopsis Termopsidis. J Gen Microbiol 113:417–420

    CAS  Google Scholar 

  • Yoshimura T (1995) Contribution of the protozoan fauna to nutritional physiology of the lower termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Wood Res 82:68–129

    Google Scholar 

  • Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554

    Article  PubMed  CAS  Google Scholar 

  • 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 395:29–39

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman PR, Greenberg JP, Wandiga SO, Crutzen PJ (1982) Termites: A potentially large source of atmospheric methane, carbon dioxide, and molecular hydrogen. Science 218:563–565

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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

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Authors and Affiliations

  1. Department of Biogeochemistry, Max Planck Institute for Terrestrial Microbiology, 35043, Marburg, Germany

    Andreas Brune

  2. Microbe Division, (Japan Collection of Microorganisms), RIKEN Bioresource Center, Saitama, 351-0198, Japan

    Moriya Ohkuma

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  1. Andreas Brune
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  2. Moriya Ohkuma
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Correspondence to Andreas Brune .

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Editors and Affiliations

  1. School of Biological & Chemical Sciences, Queen Mary University of London, Mile End Rd., London, E1 4NS, United Kingdom

    David Edward Bignell

  2. Behavioural & Evolutionary Ecology, Université Libre de Bruxelles, Av. F.D. Roosevelt 50, Bruxelles, 1050, Belgium

    Yves Roisin

  3. School of Biological Sciences, University of Sydney, Sydney, 2006, New South Wales, Australia

    Nathan Lo

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Brune, A., Ohkuma, M. (2010). Role of the Termite Gut Microbiota in Symbiotic Digestion. In: Bignell, D., Roisin, Y., Lo, N. (eds) Biology of Termites: a Modern Synthesis. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3977-4_16

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