Abstract
Termites thrive in great abundance in terrestrial ecosystems and play important roles in biorecycling of lignocellulose. Together with their microbial symbionts, they efficiently decompose lignocellulose. In so-called lower termites, a dual decomposing system, consisting of the termite's own cellulases and those of its gut protists, was elucidated at the molecular level. Higher termites degrade cellulose apparently using only their own enzymes, because of the absence of symbiotic protists. Termite gut prokaryotes efficiently support lignocellulose degradation. However, culture-independent molecular studies have revealed that the majority of these gut symbionts have not yet been cultivated, and that the gut symbiotic community shows a highly structured spatial organization. In situ localization of individual populations and their functional interactions are important to understand the nature of symbioses in the gut. In contrast to cellulose, lignin degradation does not appear to be important in the gut of wood-feeding termites. Soil-feeding termites decompose humic substances in soil at least partly, but little is known about the decomposition. Fungus-growing termites are successful in the almost complete decomposition of lignocellulose in a sophisticated cooperation with basidiomycete fungi cultivated in their nest. A detailed understanding of efficient biorecycling systems, such as that for lignocellulose, and the symbioses that provide this efficiency will benefit applied microbiology and biotechnology.
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References
Abe T, Bignell DE, Higashi M (2000) Termites: evolution, sociality, symbiosis, ecology. Kluwer, Dordrecht
Bauer S, Tholen A, Overman J, Brune A (2000) Characterization of abundance and diversity of lactic acid bacteria in the hindgut of wood- and soil-feeding termites by molecuar and culture-dependent techniques. Arch Microbiol 173:126–137
Berchtold M, König H (1995) Phylogenetic position of the two uncultivated trichomonads Pentatrichomonoides scora Kirby and Metadevescovina extranea Kirby from the hindgut of the termite Mastotermes darwiniensis Froggatt. Syst Appl Microbiol 18:567–573
Berchtold M, König H (1996) Phylogenetic analysis and in situ identification of uncultivated spirochetes from the hindgut of the termite Mastotermes darwiniensis. Syst Appl Microbiol 19:66–73
Berchtold M, Chatzinotas A, Schönhuber W, Brune A, Amann R, Hahn D, König H (1999) Differential enumeration and in situ localization of microorganisms in the hindgut of the lower termite Mastotermes darwiniensis by hybridization with rRNA-targeted probes. Arch Microbiol 172:407–416
Bignell DE, Eggleton P (1995) On the elevated intestinal pH of higher termites (Isoptera: Termitidae). Insectes Soc 42:57–69
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
Brauman A, Dore J, Eggleton P, Bignell DE, Breznak JA, Kane MD (2001) Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol Ecol 35:27–36
Breznak JA (1994) Acetogenesis from carbon dioxide in termite guts. In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York, pp 303–330
Breznak JA (2002) A need to retrieve the not-yet-cultured majority. Environ Microbiol 4:4–5
Breznak JA, Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39:453–487
Brune A (1998) Termite guts: the world's smallest bioreactors. Trends Biotechnol 16:16–21
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
Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3:263–269
Brune A, Miambi E, Breznak JA (1995) 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
Dacks JB, Silberman JD, Simpson AGB, Moriya S, Kudo T, Ohkuma M, Redfield RJ (2001) Oxymonads are closely related to the excavate taxon Trimastix. Mol Biol Evol 18:1034–1044
Dolan MF (2001) Speciation of termite gut protists: the role of bacterial symbionts. Int Microbiol 4:203–208
Dyer BD (2002) Termite hindgut symbionts. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer , Dordrecht, pp 703–713
Friedrich MW, Schmitt-Wagner D, Lueders T, Brune A (2001) Axial differences in community structure of Crenarchaeota and Euryarchaeota in the highly compartmentalized gut of the soil- feeding termite Cubitermes orthognathus. Appl Environ Microbiol 67:4880–4890
Fröhlich J, König H (1999a) Ethidium bromide: a fast fluorescent staining procedure for the detection of symbiotic partnership of flagellates and prokaryotes. J Microbiol Methods 35:121–127
Fröhlich J, König H (1999b) Rapid isolation of single microbial cells from mixed natural and laboratory populations with the aid of a micromanipulator. Syst Appl Microbiol 22:249–157
Gerbod D, Edgcomb VP, Nöel C, Delgado-Viscogliosi P, Viscogliosi E (2000) Phylogenetic position of parabasalid symbionts from the termite Calotermes flavicollis based on small subunit rRNA sequences. Int Microbiol 3:165–172
Hinze B, Crailsheim K, Leuthold RH (2002) Polyethism in food processing and social organisation in the nest of Macrotermes bellicosus (Isoptera, Termitidae). Insectes soc 49:31–37
Hopkins DW, Chudek JA, Bignell DE, Frouz J, Webster EA, Lawson T (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
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 Biol Biochem 32:653–658
Iida T, Ohkuma M, Ohtoko K, Kudo T (2000) Symbiotic spirochetes in the termite hindgut: phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiol Ecol 34:17–26
Inoue T, Murashima K, Azuma J-I, Sugimoto A, Slaytor M (1997) Cellulose and xylan utilization in the lower termite Reticulitermes speratus. J Insect Physiol 43:235–242
Itakura S, Tanaka H, Enoki A (1997) Distribution of cellulases, glucose and related substances in the body of Coptotermes formosanus. Mater Organismen 31:17–29
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
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
Keeling PJ, Poulsen N, McFadden GI (1998) Phylogenetic diversity of parabasalian symbionts from termites, including the phylogenetic position of Pseudotrypanosoma and Trichonympha. J Eukaryot Microbiol 45:643–650
König H, Fröhlich J, Berchtold M, Wenzel M (2002) Diversity and microhabitats of the hindgut flora of termites. Recent Res Devel Microbiol 6:125–156
Kosono S, Maeda M, Fuji F, Arai H, Kudo T (1997) Three of the seven bphC genes of Rhodococcus erythropolis TA421, isolated from a termite ecosystem, are located on an indigenous plasmid associated with biphenyl degradation. Appl Environ Microbiol 63:3282–3285
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
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
Kuhnigk T, Borst E-M, Ritter A, Kämpfer P, Graf A, Hertel H, König H (1994) Degradation of lignin monomers by the hindgut flora of xylophagous termites. Syst Appl Microbiol 17:76–85
Kuhnigk T, Branke J, Krekeler D, Cypionka H, König H (1996) A feasible role of sulfate-reducing bacteria in the termite gut. Syst Appl Microbiol 19:139–149
Leadbetter JR, Breznak JA (1996) Physiological ecology of Methanobrevibacter cuticularis sp. nov and Methanobrevibacter curvagus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes. Appl Environ Microbiol 62:3620–3631
Leadbetter JR, Crosby LD, Breznak A (1998) Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch Microbiol 169:287–292
Leadbetter JR, Schmidt TM, Graber JR, Breznak JA (1999) Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283:686–689
Lilburn TG, Schmidt TM, Breznak JA (1999) Phylogenetic diversity of termite gut spirochaetes. Environ Microbiol 1:331–345
Lilburn TG, Kim KS, Ostrom NE, Byzek KR, Leadbetter JR, Breznak JA (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498
Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa K, et al (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804
Maeda M, Chung S-Y, Song E, Kudo T (1995) Multiple genes encoding 2,3-dihydroxybiphenyl 1,2-dioxygenase in the gram-positive polychlorinated biphenyl-degrading bactterium Rhodococcus erythropolis TA421, isolated from a termite ecosystem. Appl Environ Microbiol 61:549–555
Moriya S, Tanaka K, Ohkuma M, Sugano S, Kudo T (2001) Diversification of the microtubule system in the early stage of eukaryote evolution: elongation factor 1α and α-tubulin protein phylogeny of termite symbiotic oxymonad and hypermastigote protists. J Mol Evol 51:6–16
Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma J-I (2002) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32:777–784
Noda S, Ohkuma M, Usami R, Horikoshi K, Kudo T (1999) Culture-independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis. Appl Environ Microbiol 65:4935–4942
Noda S, Ohkuma M, Kudo T (2002) Nitrogen fixation genes expressed in the symbiotic microbial community in the gut of the termite Coptotermes formosanus. Microb Environ 17:139–143
Ohkuma M (2002) Symbiosis in the termite gut—culture-independent molecular approaches. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer, Dordrecht, pp 717–730
Ohkuma M, Kudo, T (1996) Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl Environ Microbiol 62:461–468
Ohkuma M, Iida T, Kudo T (1999a) Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites. FEMS Microbiol Lett 181:123–129
Ohkuma M, Noda S, Kudo T (1999b) Phylogeny of symbiotic methanogenes in diverse termites. FEMS Microbiol Lett 171:147–153
Ohkuma M, Noda S, Kudo T (1999c) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65:4926–4934
Ohkuma M, Ohtoko K, Iida T, Tokura M, Moriya S, Usami R, Horikoshi K, Kudo T (2000) Phylogenetic identification of hypermastigotes, Pseudotrichonympha, Spirotrichonympha, Holomastigotes, and parabasalian symbionts in the hindgut of termites. J Eukaryot Microbiol 47:249–259
Ohkuma M, Noda S, Hongoh Y, Kudo T (2002) Diverse bacteria related to the bacteroides subgroup of the CFB phylum within the gut symbiotic community of various termites. Biosci Biotech Biochem 66:78–84
Ohtoko K, Ohkuma M, Moriya S, Inoue T, Usami R, Kudo T (2000) Diverse genes of cellulase homologues of glycosyl hydrolase family 45 from the symbiotic protists in the hindgut of the termite Reticulitermes speratus. Extremophiles 4: 343–349
Paster BJ, Dewhirst FE, Cooke SM, Fussing V, Poulsen LK, Breznak JA (1996) Phylogeny of not-yet-cultured spirochetes from termite guts. Appl Environ Microbiol 62:347–352
Pointing SB (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57:20–33
Prillinger H, Messner R, König H, Bauer R, Lopandic K, Molnar O, Dangel P, Weigang F, Kirisits T, Nakase T, Sigler L (1996) Yeasts associated with termites: a phenotypic and genotypic characterization and use of coevolution for dating evolutionary radiations in asco- and basidiomycetes. Syst Appl Microbiol 19:265–283
Radek R (1999) Flagellates, bacteria and fungi associated with termites: diversity and function in nutrition. Ecotropica 5:183–196
Rouland-Lefèvre C, Bignell DE (2002) Cultivation of symbiotic fungi by termites of the subfamily Macrotermitinae. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer , Dordrecht, pp 733-756
Rouland-Lefèvre C, Diouf MN, Brauman A, Neyra M (2002) Phylogenetic relationships in Termitomyces (Family Agaricaceae) based on the nucleotide sequence of ITS: a first approach to elucidate the evolutionary history of the symbiosis between fungus-growing termites and their fungi. Mol Phylogenet Evol 22:423–429
Schäfer A, Konrad R, Kuhnigk T, Kämpfer P, Hertel H, König H (1996) Hemicellulose-degrading bacteria and yeasts from the termite gut. J Appl Bacteriol 80:471–478
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
Shinzato N, Matsumoto T, Yamaoka I, Oshima T, Yamagishi A (1999) Phylogenetic diversity of symbiotic methanogens living in the hindgut of the lower termite Reticulitermes speratus analyzed by PCR and in situ hybridization. Appl Environ Microbiol 65:837–840
Shinzato N, Matsumoto T,Yamaoka I, Oshima T, Yamagishi A (2001) Methanogenic symbionts and the locality of other host lower termites. Microb Environ 16:43–47
Slaytor M (1992) Cellulose digestion in termites and cockroaches; do symbionts play a role? Comp Biochem Phys 103B:775–784
Slaytor M, Veivers PC, Lo N (1997) Aerobic and anaerobic metabolism in the higher termite Nasutitermes walkeri (Hill). Insect Biochem Mol Biol 27:291-303
Taprab Y, Ohkuma M, Johjima T, Maeda Y, Moriya S, Inoue T, Suwanarit P, Noparatnaraporn N, Kudo T (2002) Molecular phylogeny of symbiotic basidiomycetes of fungus-growing termites in Thailand and their relationship with the host. Biosci Biotech Biochem 66:1159–1163
Tayasu I, Inoue T, Miller LR, Sugimoto A, Takeichi S, Abe T (1998) Confirmation of soil-feeding termites (Isoptera: Termitidae: Termitinae) in Australia using stable isotope ratios. Functional Ecol 12:536–542
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
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
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
Tokuda G, Lo N, Watanabe H, Slaytor M, Matsumoto T, Noda H (1999) Metazoan cellulase genes from termites: intron/exon structures and sites of expression. Biochim Biophys Acta 1447:146–159
Tokura M, Ohkuma M, Kudo T (2000) Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites. FEMS Microbiol Ecol 33:233–240
Varma A, Kolli BK, Paul J, Saxena S, König H (1994) Lignocellulose degradation by microorganisms from termite hills and termite guts. A survey on the present state of art. FEMS Microbiol Rev 15:9–28
Watanabe H, Tokuda G (2001) Animal cellulases. Cell Mol Life Sci 58:1167–1178
Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331
Wenzel M, Schönig I, Berchtold M, Kämpfer P, König H (2002) Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92:32–40
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The work of my group was supported by grants to the Bioarchitect Research Program and the Eco Molecular Science Research Program from RIKEN.
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Ohkuma, M. Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61, 1–9 (2003). https://doi.org/10.1007/s00253-002-1189-z
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DOI: https://doi.org/10.1007/s00253-002-1189-z