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Applied Microbiology and Biotechnology

, Volume 97, Issue 18, pp 7943–7962 | Cite as

The cellulolytic system of the termite gut

  • Helmut König
  • Li Li
  • Jürgen Fröhlich
Mini-Review

Abstract

The demand for the usage of natural renewable polymeric material is increasing in order to satisfy the future needs for energy and chemical precursors. Important steps in the hydrolysis of polymeric material and bioconversion can be performed by microorganisms. Over about 150 million years, termites have optimized their intestinal polysaccharide-degrading symbiosis. In the ecosystem of the “termite gut,” polysaccharides are degraded from lignocellulose, such as cellulose and hemicelluloses, in 1 day, while lignin is only weakly attacked. The understanding of the principles of cellulose degradation in this natural polymer-degrading ecosystem could be helpful for the improvement of the biotechnological hydrolysis and conversion of cellulose, e.g., in the case of biogas production from natural renewable plant material in biogas plants. This review focuses on the present knowledge of the cellulose degradation in the termite gut.

Keywords

Cellulose Cellulases Glycolytic enzymes Termites Gut microbiota 

Notes

Acknowledgments

We thank the Deutsche Forschungsgemeinschaft, the Environment Centre of the Johannes Gutenberg-University (Mainz) and the Federal Ministry of Food, Agriculture and Consumer Protection via Fachagentur für Nachwachsende Rohstoffe (FNR) e.V. for financial support.

References

  1. Aanen DK, Eggleton P (2005) Fungus-growing termites originated in African rain forest. Curr Biol 15:851–855PubMedCrossRefGoogle Scholar
  2. Aanen DK, Ros VID, Licht HHD, Mitchell J, de Beer ZW, Slippers B, Rouland-LeFevre C, Boomsma JJ (2007) Patterns of interaction specificity of fungus-growing termites and Termitomyces symbionts in South Africa. BMC Evol Biol 7:115. doi: 10.1186/1471-2148-7-115 PubMedCrossRefGoogle Scholar
  3. Abe T, Bignell DE, Higashi M (eds) (2000) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, DordrechtGoogle Scholar
  4. Abt B, Han C, Scheuner C, Lu MG, Lapidus A, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng JF, Tapia R, Goodwin LA, Pitluck S, Liolios K, Pagani I, Ivanova N, Mavromatis K, Mikhailova N, Hunte-mann M, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Brambilla EM, Rohde M, Spring S, Gronow S, Goker M, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Detter JC (2012) Complete genome sequence of the termite hindgut bacterium Spirochaeta coccoides type strain (SPN1(T)), reclassification in the genus Sphaerochaeta as Sphaerochaeta coccoides comb. nov and emendations of the family Spirochaetaceae and the genus Sphaerochaeta. Stand Genomic Sci 6:194–209PubMedCrossRefGoogle Scholar
  5. Bakalidou A, Kämpfer P, Berchtold M, Kuhnigk T, Wenzel M, König H (2002) Cellulosimicrobium variable sp. nov., a cellulolytic bacterium from the hindgut of the termite Mastotermes darwiniensis. Int J Syst Evol Microbiol 52:1185–1192PubMedCrossRefGoogle Scholar
  6. 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 173:126–137PubMedCrossRefGoogle Scholar
  7. Bayer EA, Chanzy H, Lamed R, Shoham Y (1998) Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol 8:548–557PubMedCrossRefGoogle Scholar
  8. Beckwith TD, Rose EJ (1929) Cellulose digestion by organisms from the termite gut. Proc Soc Exp Biol Med 27:4–6CrossRefGoogle Scholar
  9. Béguin P, Lemaire M (1996) The cellulosome: an exocellular, multiprotein complex specialized in cellulose degradation. Crit Rev Biochem Mol Biol 31:201–236PubMedCrossRefGoogle Scholar
  10. Berchtold M, König H (1995) Phylogenetic position of two uncultivated trichomonads Pentatrichomonoides scroa Kirby and Metadevescovina extranea Kirby from the hindgut of the termite Mastotermes darwiniensis Froggatt. Syst Appl Microbiol 18:567–573CrossRefGoogle Scholar
  11. 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 19:66–73CrossRefGoogle Scholar
  12. Berchtold M, Ludwig W, König H (1994) 16S rDNA sequence and phylogenetic position of an uncultivated spirochete from the hindgut of the termite Mastotermes darwiniensis Froggatt. FEMS Microbiol Lett 123:269–274PubMedCrossRefGoogle Scholar
  13. Berchtold M, Breunig A, König H (1995) Culture and phylogenetic characterization of Trichomitus trypanoides Duboscque & Grassè 1924, n. comb.: a trichomonad flagellate isolated from the hindgut of the termite Reticulitermes santonensis Feytaud. J Eukaryot Microbiol 42:388–391PubMedCrossRefGoogle Scholar
  14. 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. Arch Microbiol 172:407–416PubMedCrossRefGoogle Scholar
  15. Bignell DE, Oskarsson H, Anderson JM (1980a) Specialization of the hindgut wall for the attachment of symbiotic microorganisms in a termite—Procubitermes aburiensis (Isoptera, Termitidae, Termitinae). Zoomorphology 96:103–112CrossRefGoogle Scholar
  16. Bignell DE, Oskarsson H, Anderson JM (1980b) Distribution and abundance of bacteria in the gut of a soil-feeding termite Procubitermes aburiensis (Termitidae, Termitinae). J Gen Microbiol 117:393–403PubMedGoogle Scholar
  17. Bignell DE, Slaytor M, Veivers PC, Muhlemann R, Leuthold RH (1994) Functions of symbiotic fungus gardens in higher termites of the genus Macrotermes: evidence against the acquired enzyme hypothesis. Acta Microbiol Immunol Hung 41:391–401PubMedGoogle Scholar
  18. Blättel V, Larisika M, Nowak C, Eich A, Eckelt J, König H (2011) β-1,3-Glucanase from Delftia tsuruhatensis strain MV01 and its potential application in vinification. J Appl Environ Microbiol 77:983–990CrossRefGoogle Scholar
  19. 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
  20. Botha TC, Hewitt PH (1979) A study of the gut morphology and some physiological observations on the influence of a diet of green Themeda triandra on the harvester termite Hodotermes mossambicus (Hagen). Phytophylactica 11:57–60Google Scholar
  21. Braumann A, Koenig JF, Dutreix J, Garcia JL (1990) Characterization of two sulfate-reducing bacteria from the gut of the soil-feeding termite, Cubitermes speciosus. Antonie Leeuw 58:271–275CrossRefGoogle Scholar
  22. Braumann A, Kane MD, Labat M, Breznak JA (1992) Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384–1386CrossRefGoogle Scholar
  23. Braumann A, Dore J, Eggleton P, Bignell D, Breznak JA, Kane MD (2001) Molecular phylogenetic profiling of prokaryote communities in guts of termites with different feeding habits. FEMS Microbiol Ecol 35:27–36CrossRefGoogle Scholar
  24. Breznak JA (1975) Symbiotic relationships between termites and their intestinal microbiota. Symp Soc Exp Biol 29:559–580PubMedGoogle Scholar
  25. Breznak JA (1982) Intestinal microbiota of termites and other xylophagous insects. Annu Rev Microbiol 36:323–343PubMedCrossRefGoogle Scholar
  26. Breznak JA (1984) Biochemical aspects of symbiosis between termites and their intestinal microbiota. In: Anderson JM, Rayner ADM, Walton DWH (eds) Invertebrate microbial interactions. Cambridge University Press, Cambridge, pp 173–203Google Scholar
  27. Breznak JA (1994) Acetogenesis from carbon dioxide in termite guts. In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York, pp 303–330CrossRefGoogle Scholar
  28. Breznak JA, Blum JS (1991) Mixotrophy of the termite gut acetogen, Sporomusa termitida. Arch Microbiol 156:105–110CrossRefGoogle Scholar
  29. Breznak JA, Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39:453–487CrossRefGoogle Scholar
  30. Breznak JA, Pankratz HS (1977) In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus (Shiraki)]. Appl Environ Microbiol 33:406–426PubMedGoogle Scholar
  31. Breznak JA, Switzer JM (1986) Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl Environ Microbiol 52:623–630PubMedGoogle Scholar
  32. Breznak JA, Switzer JM, Seitz HJ (1988) Sporomusa termitida sp. nov., an H2/CO2-utilizing acetogen isolated from termites. Arch Microbiol 150:282–288CrossRefGoogle Scholar
  33. Brugerolle G (2000) A microscopic investigation of the genus Foaina, a parabasalid protist symbiotic in termites and phylogenetic considerations. Eur J Protistol 36:20–28CrossRefGoogle Scholar
  34. Brugerolle G, König H (1997) Ultrastructure and organisation of the cytoskeleton in Oxymonas, an intestinal flagellate of termites. J Eukaryot Microbiol 44:305–313CrossRefGoogle Scholar
  35. Brugerolle G, Lee JJ (2000a) Phylum Parabasalia. In: Lee JJ, Leedale GF, Bradbury P (eds) The illustrated guide to the protozoa, second edition, vols 1 and 2. Society of Protozoologists, Lawrence, pp 1196–1250Google Scholar
  36. Brugerolle G, Lee JJ (2000b) Order Oxymonadida. In: Lee JJ, Leedale GF, Bradbury P (eds) The illustrated guide to the protozoa, vol 2, 2nd edn. Society of Protozoologists, Lawrence, pp 1186–1195Google Scholar
  37. Brugerolle G, Radek R (2006) Symbiotic protozoa of termites. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Heidelberg, pp 243–269CrossRefGoogle Scholar
  38. Brugerolle G, Breunig A, König H (1994) Ultrastructural study of Pentatrichomonoides sp., a trichomonad flagellate from Mastotermes darwiniensis. Eur J Protistol 30:372–378CrossRefGoogle Scholar
  39. Brummell DA, Catala C, Lashbrook CC, Bennett AB (1997) A membrane-anchored E-type endo-1,4-β-glucanase is localized on Golgi and plasma membranes of higher plants. Proc Natl Acad Sci U S A 94:4794–4799PubMedCrossRefGoogle Scholar
  40. Brune A (1998) Termite guts: the world’s smallest bioreactors. TIBTECH 16:16–21CrossRefGoogle Scholar
  41. Brune A (2007) Microbiology: woodworker's digest. Nature 450:487–488PubMedCrossRefGoogle Scholar
  42. Brune A, Emerson D, Kühl MJ, Breznak A (1995) The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl Environ Microbiol 61:2681–2687PubMedGoogle Scholar
  43. Byrne KA, Lehnert SA, Johnson SE, Moore SS (1999) Isolation of a cDNA encoding a putative cellulase in the red claw crayfish Cherax quadricarinatus. Gene 239:317–324PubMedCrossRefGoogle Scholar
  44. Cho MJ, Kim YH, Shin K, Kim YK, Kim YS, Kim TJ (2010) Symbiotic adaptation of bacteria in the gut of Reticulitermes speratus: low endo-beta-1,4-glucanase activity. Biochem Biophys Res Commun 395:432–435PubMedCrossRefGoogle Scholar
  45. Cleveland LR (1924) The physiological and symbiotic relationships between the intestinal protozoa of termites and their hosts, with special reference to Reticulitermes flavipes Kollar. Biol Bull 46:117–127Google Scholar
  46. Cleveland LR, Grimstone AV (1964) The fine structure of the flagellate Mixotricha paradoxa and its associated microorganisms. Proc R Soc Lond Ser B 159:668–686CrossRefGoogle Scholar
  47. Colombo AL, Padovan ACB, Chaves GM (2011) Current knowledge of Trichosporon spp. and Trichosporonosis. Clin Microbiol Rev 24:682–700PubMedCrossRefGoogle Scholar
  48. Conrad R (1984) Methanemission aus Termitennestern. Naturwiss Rundsch 37:412–413Google Scholar
  49. Cypionka H (2000) Oxygen respiration by Desulfovibrio species. Ann Rev Microb 54:827–848PubMedCrossRefGoogle Scholar
  50. Czolij R, Slaytor M, O'Brien RW (1985) Bacterial flora of the mixed segment and the hindgut of the higher termite Nasutitermes exitiosus Hill (Termitidae: Nasutitermitinae). Appl Environ Microbiol 49:1226–1236Google Scholar
  51. Dacks JB, Redfield RJ (1998) Phylogenetic placement of Trichonympha. J Eukaryot Microbiol 45:445–447PubMedCrossRefGoogle Scholar
  52. Davison A, Blaxter M (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22:1273–1284PubMedCrossRefGoogle Scholar
  53. Delgado-Viscogliosi P, Viscogliosi E, Gerbod D, Kulda J, Sogin ML, Edgcomb VP (2000) Molecular phylogeny of parabasalids based on small subunit rRNA sequences, with emphasis on the Trichomonadinae subfamily. J Eukaryot Microbiol 47:70–75PubMedCrossRefGoogle Scholar
  54. Delmer DP, Amor Y (1995) Cellulose biosynthesis. Plant Cell 7:987–1000PubMedGoogle Scholar
  55. Dickman A (1931) Studies on the intestinal flora of termites with reference to the ability to digest cellulose. Biol Bull 61:85–92CrossRefGoogle Scholar
  56. Dröge S, Limper U, Emtiazi F, Schönig I, Pavlus N, Drzyzga O, Fischer U, König H (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
  57. 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 172:392–397CrossRefGoogle Scholar
  58. Dröge S, Rachel R, Radek R, König H (2008) Treponema isopterocolens sp. nov., a novel spirochete from the hindgut of the termite Incisitermes tabogae. Int J Syst Evol Microbiol 58:1079–1083PubMedCrossRefGoogle Scholar
  59. Dyer BD, Khalsa O (1993) Surface bacteria of Streblomastix strix are sensory symbionts. Biosystems 31:169–180PubMedCrossRefGoogle Scholar
  60. 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
  61. EREC (2004) Renewable energy scenario to 2040. http://www.censolar.es/erec2040.pdf
  62. Esenther GR, Kirk TK (1974) Catabolism of aspen sapwood by Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 67:989–999Google Scholar
  63. Eutick ML, O'Brien RW, Slaytor M (1978) Bacteria from the gut of Australian termites. Appl Environ Microbiol 35:823–828PubMedGoogle Scholar
  64. Fengel D, Wegener G (1984) Wood. Chemistry, ultrastructure, reactions. Walter de Gruyter, BerlinGoogle Scholar
  65. Fittkau J, Klinge H (1973) On biomass and trophic structure of the central Amazonian rain forest ecosystem. Biotropica 5:2–14CrossRefGoogle Scholar
  66. FNR (ed) (2009) Biogas-Messprogramm II. Media Cologne Kommunikationsmedien GmbH, HürthGoogle Scholar
  67. Fröhlich J, König H (1999) Rapid isolation of single microbial cells from mixed natural and laboratory populations with the aid of a micromanipulator. Syst Appl Microbiol 22:249–257PubMedCrossRefGoogle Scholar
  68. Fröhlich J, König H (2000) New techniques for the isolation of single prokaryotic cells. FEMS Microbiol Rev 24:567–572PubMedCrossRefGoogle Scholar
  69. Fröhlich J, Sass H, Babenzien HD, Kuhnigk T, Varma A, Saxena S, Nalepa C, Pfeiffer P, König H (1999) Isolation of Desulfovibrio intestinalis sp. nov., from the hindgut of the lower termite Mastotermes darwiensis. Can J Microbiol 45:145–152PubMedGoogle Scholar
  70. Geib SM, Filley TR, Hatcher PG, Hoover K, Carlson JE, Jimenez-Gasco Mdel M, Nakagawa-Izumi A, Sleighter RL, Tien M (2008) Lignin degradation in wood-feeding insects. Proc Natl Acad Sci U S A 105:12932–12937PubMedCrossRefGoogle Scholar
  71. 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
  72. Gujjari P, Suh SO, Lee CF, Zhou JJ (2011) Trichosporon xylopini sp. nov., a hemicellulose-degrading yeast isolated from the wood-inhabiting beetle Xylopinus saperdioides. Int J Syst Evol Microbiol 61:2538–2542PubMedCrossRefGoogle Scholar
  73. Hackstein JHP, Stumm CK (1994) Methane production in terrestrial arthropods. Proc Natl Acad Sci U S A 91:5441–5445PubMedCrossRefGoogle Scholar
  74. Hackstein JHP, Langer P, Rosenberg J (1996) Genetic and evolutionary constraints for symbiosis between animals and methanogenic bacteria. Environ Monit Assess 42:39–56CrossRefGoogle Scholar
  75. Haifig I, Leonardo FC, Costa FF, Costa-Leonardo AM (2012) On the apterous line of the termite Velocitermes heteropterus (Isoptera: Termitidae): developmental pathways and cellulose digestion. Zool Sci 29:815–820PubMedCrossRefGoogle Scholar
  76. He S, Ivanova N, Kirton E, Allgaier M, Bergin C, Scheffrahn RH, Kyrpides NC, Warnecke F, Tringe SG, Philip Hugenholtz P (2013) Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood- and dung-feeding higher termites. PLoS One 8:e61126PubMedCrossRefGoogle Scholar
  77. Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644PubMedCrossRefGoogle Scholar
  78. Henrissat B, Claeyssens M, Tomme P, Lemesle L, Mornon JP (1989) Cellulase families revealed by hydrophobic cluster analysis. Gene 81:83–95PubMedCrossRefGoogle Scholar
  79. 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
  80. Hirayama K, Watanabe H, Tokuda G, Kitamoto K, Arioka M (2010) Purification and characterization of termite endogenous beta-1,4-endoglucanases produced in Aspergillus oryzae. Biosci Biotechnol Biochem 74:1680–1686PubMedCrossRefGoogle Scholar
  81. Hogan ME, Schulz MW, Slaytor M, Czolij RT, O'Brien RW (1988) Components of termite and protozoal cellulases from the lower termite, Coptotermes lacteus Froggatt. Insect Biochem 18:45–51CrossRefGoogle Scholar
  82. Honigberg BM (1970) Protozoa associated with termites and their role in digestion. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic, New York, pp 1–36Google Scholar
  83. Huntenburg W, Stockert L, Smith-Somerville HE, Buhse HE (1986) Trichomitus trypanoides (Trichomonadida) from the termite Reticulitermes flavipes. 1. In vitro cultivation and cloning. Trans Am Microsc Soc 105:211–222CrossRefGoogle Scholar
  84. 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 34:17–26PubMedCrossRefGoogle Scholar
  85. Inoue T, Murashima K, Azuma JI, Sugimoto A, Slaytor M (1997) Cellulose and xylan utilization in the lower termite Reticulitermes speratus. J Insect Physiol 43:235–242PubMedCrossRefGoogle Scholar
  86. 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
  87. Itakura S, Ueshima K, Tanaka H, Enoki A (1995) Degradation of wood components by subterranean termite, Coptotermes formosanus Shiraki. Mokuzai Gakkaishi 41:580–586Google Scholar
  88. Itakura S, Tanaka H, Enoki A (1997) Distribution of cellulases, glucose and related substances in the body of Coptotermes formosanus. Mater Organismen 31:17–29Google Scholar
  89. Itakura S, Masuta T, Tanaka H, Enoki A (2006) Identification of two subterranean termite species (Isoptera: Rhinotermitidae) using cellulase genes. J Econ Entomol 99:123–128Google Scholar
  90. James R, Nguyen T, Arthur W, Levine K, Willams DC (1997) Hydrolase (beta-glucanase alpha-glucanase and protease) activity in Ariolimax columbianus (banana slug) and Arion ater (garden slug). Comp Biochem Physiol 118B:275–283Google Scholar
  91. Kane MD, Breznak JA (1991) Acetonema longum gen. sp. nov., an H2/CO2 acetogenic bacterium from the termite, Pterotermes occidentis. Arch Microbiol 156:91–98PubMedCrossRefGoogle Scholar
  92. Kane MD, Baumann A, Breznak JA (1991) Clostridium mayombei sp. nov., an H2/CO2 acetogenic bacterium from the gut of the African soil-feeding termite, Cubitermes speciosus. Arch Microbiol 156:99–104CrossRefGoogle Scholar
  93. Keeling P, Poulsen N, McFadden GI (1998) Phylogenetic diversity of parabasalian symbionts from termites, including the phylogenetic position of Pseudotrypanosoma and Trichonympha. J Eukaryot Microbiol 45:643–650PubMedCrossRefGoogle Scholar
  94. Khademi S, Guarino LA, Watanabe H, Tokuda G, Meyer EF (2002) Structure of an endoglucanase from termite, Nasutitermes takasagoensis. Acta Crystallogr D: Biol Crystallogr 58:653–659CrossRefGoogle Scholar
  95. Kim DW, Jeong YK, Jang YH, Lee JK (1994) Purification and characterisation of endoglucanase components from Trichoderma viride. J Ferment Bioeng 77:363–360Google Scholar
  96. Kim N, Choo YM, Lee KS, Hong SJ, Seol KY, Je YH, Sohn HD, Jin BR (2008) Molecular cloning and characterization of a glycosyl hydrolase family 9 cellulase distributed throughout the digestive tract of the cricket Teleogryllus emma. Comp Biochem Physiol B Biochem Mol Biol 150:368–376PubMedCrossRefGoogle Scholar
  97. Kitade O, Matsumoto T (1998) Characteristics of the symbiotic flagellate composition within the termite family Rhinotermitidae. Symbiosis 25:271–278Google Scholar
  98. Köhler T, Dietrich C, Scheffrahn RH, Brune A (2012) High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl Environ Microbiol 78:4691–4701PubMedCrossRefGoogle Scholar
  99. König H, Dröge S (2010) Intestinal spirochetes of termites. In: Dubinsky Z, Seckbach J (eds) All flesh is grass: plant–animal interactions. Springer, Heidelberg, pp 67–89Google Scholar
  100. König H, Varma A (eds) (2006) Intestinal microorganisms of termites and other invertebrates. Springer, HeidelbergGoogle Scholar
  101. König H, Fröhlich J, Berchtold M, Wenzel M (2002) Diversity and microhabitats of the hindgut flora of termites. Recent Res Dev Microb 6:125–156Google Scholar
  102. König H, Fröhlich J, Hertel H (2006) Diversity and lignocellulolytic activities of cultured microorganisms. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Heidelberg, pp 271–301Google Scholar
  103. König H, Fröhlich J, Li L, Wenzel M, Dröge S, Breunig A, Pfeiffer P, Radek R, Brugerolle G (2007) The flagellates of the Australian termite Mastotermes darwiniensis: identification of their symbiotic bacteria and cellulases. Symbiosis 44:51–65Google Scholar
  104. Korish M (2003) Production, purification, properties and application of the cellulases from a wild type strain of a yeast isolate. Thesis, University MainzGoogle Scholar
  105. Krasil'nikov NA, Satdykov SI (1969) Estimation of the total bacteria in the intestines of termites. Microbiology 38:289–292Google Scholar
  106. Krishna K (1970) Taxonomy, physiology, and distribution of termites. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic, New York, pp 127–152Google Scholar
  107. Krishna K, Weesner FM (eds) (1969) Biology of termites. vol. 1. Academic, New YorkGoogle Scholar
  108. Krishna K, Weesner FM (eds) (1970) Biology of termites, vol. 2. Academic, New YorkGoogle Scholar
  109. 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 2:151–161CrossRefGoogle Scholar
  110. Kuhnigk T, Borst EM, Breunig A, König H, Collins MP, Hutson RA, Kämpfer P (1995) Bacillus oleronius sp. nov., a member of the hindgut flora of the termite Reticulitermes santonensis. Can J Microbiol 41:699–706PubMedCrossRefGoogle Scholar
  111. Kuhnigk T, Branke J, Krekeler D, Cypionka H, König H (1996) A feasible role of sulfate-reducing bacteria in the termite gut. System Appl Microbiol 19:139–149CrossRefGoogle Scholar
  112. Kundu RK, Dube S, Dube DK (1988) Extracellular cellulolytic enzyme system of Aspergillus japonicus: 3. Isolation, purification and characterization of multiple forms of endoglucanase. Enzym Microb Technol 10:100–109CrossRefGoogle Scholar
  113. Kwon I, Ekino K, Goto M, Furukawa K (1999) Heterologous expression and characterization of endoglucanase I (EGI) from Trichoderma viride HK-75. Biosci Biotechnol Biochem 63:1714–1720PubMedCrossRefGoogle Scholar
  114. 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
  115. Leadbetter JR, Crosby LD, Breznak JA (1998) Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch Microbiol 169:287–292PubMedCrossRefGoogle Scholar
  116. Leadbetter JR, Schmidt TM, Graber JR, Breznak JA (1999) Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283:686–689PubMedCrossRefGoogle Scholar
  117. Lee SJ, Kim SR, Yoon HJ, Kim I, Lee KS, Je YH, Lee SM, Seo SJ, Dae Sohn H, Jin BR (2004) cDNA cloning, expression, and enzymatic activity of a cellulase from the mulberry longicorn beetle, Apriona germari. Comp Biochem Physiol B Biochem Mol Biol 139:107–116PubMedCrossRefGoogle Scholar
  118. Li L, Fröhlich J, Pfeiffer P, König H (2003) Termite gut symbiotic archaezoa are becoming living metabolic fossils. Eukaryot Cell 2:1091–1098PubMedCrossRefGoogle Scholar
  119. 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, Heidelberg, pp 221–241CrossRefGoogle Scholar
  120. Lilburn TG, Byzek KR, Kim KS, Breznak JA (2000) Nitrogen fixation in spirochetes. Abstr Gen Meet ASM 100:475Google Scholar
  121. Lin L, Qin G, Wei Y, Du L, Pang Z, Huang R (2009) Saturation mutagenesis of three amino acid positions consisting of the active site of an endoglucanase from termite Coptotermes formosanus. Sheng Wu Gong Cheng Xue Bao 25:927–931PubMedGoogle Scholar
  122. Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa K, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804PubMedCrossRefGoogle Scholar
  123. Lo N, Watanabe H, Sugimura M (2003) Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals. Proc Biol Sci 270(Suppl 1):S69–S72PubMedCrossRefGoogle Scholar
  124. Malburg LM, Lee JMT, Forsberg CW (1992) Cellulases. In: Winkelmann G (ed) Microbial degradation of natural products. VCH Verlagsgesellschaft mbH, Weinheim, pp 128–159Google Scholar
  125. Mannesmann R, Piechowski B (1989) Verteilungsmuster von Gärkammerbakterien einiger Termitenarten. Mater Org 24:161–177Google Scholar
  126. Martin MM (1991) The evolution of cellulose digestion in insects. Phil Trans R Soc London B 333:281–288CrossRefGoogle Scholar
  127. Martius CR, Wassmann U, Thein A, Bandeira H, Rennenberg JW, Seiler W (1993) Methane emission from wood-feeding termites in Amazonia. Chemosphere 26:623–632CrossRefGoogle Scholar
  128. McEwen SE, Slaytor M, O'Brien RW (1980) Cellobiase activity in three species of Australian termites. Insect Biochem 10:563–567CrossRefGoogle Scholar
  129. Mishra SC (1979) Studies on deterioration of wood by insects. IV. Digestibility and digestion of major wood components by the termite Neotermes bosei Snyder (Isoptera: Kalotermitidae). Mat Organismen 14:269–277Google Scholar
  130. Molnar O, Schatzmayr G, Fuchs E, Prillinger H (2004) Trichosporon mycotoxinivorans sp. nov., a new yeast species useful in biological detoxification of various mycotoxins. Syst Appl Microbiol 27:661–671PubMedCrossRefGoogle Scholar
  131. Moriya S, Ohkuma M, Kudo T (1998) Phylogenetic position of symbiotic protist Dinenympha exilis in the hindgut of the termite Reticulitermes speratus inferred from the protein phylogeny of elongation factor 1 alpha. Gene 210:221–227PubMedCrossRefGoogle Scholar
  132. Myles TG (1999) Phylogeny and taxonomy of the Isoptera. XIII Intl. Congress Intl. Union for the Study of Social Insects 29, Adelaide, Australia.Google Scholar
  133. Nakashima K, Azuma J (2000) Distribution and properties of endo-beta-1,4-glucanase from a lower termite, Coptotermes formosanus (Shiraki). Biosci Biotechnol Biochem 64:1500–1506PubMedCrossRefGoogle Scholar
  134. Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI (2002a) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32:777–784PubMedCrossRefGoogle Scholar
  135. Nakashima K, Watanabe H, Azuma JI (2002b) Cellulase genes from the parabasalian symbiont Pseudotrichonympha grassii in the hindgut of the wood-feeding termite Coptotermes formosanus. Cell Mol Life Sci 59:1554–1560PubMedCrossRefGoogle Scholar
  136. Nakatani F, Kawaguchi T, Takada G, Sumitani JI, Moriyama Y, Arai M (2000) Cloning and sequencing of an endoglucanase gene from Scopulariopsis brevicaulis TOF-1212, and its expression in Saccharomyces cerevisiae. Biosci Biotechnol Biochem 64:1238–1246PubMedCrossRefGoogle Scholar
  137. Ni J, Takehara M, Watanabe H (2005) Heterologous overexpression of a mutant termite cellulase gene in Escherichia coli by DNA shuffling of four orthologous parental cDNAs. Biosci Biotechnol Biochem 69:1711–1720PubMedCrossRefGoogle Scholar
  138. Ni J, Takehara M, Miyazawa M, Watanabe H (2007) Random exchanges of non-conserved amino acid residues among four parental termite cellulases by family shuffling improved thermostability. Protein Eng Des Sel 20:535–542PubMedCrossRefGoogle Scholar
  139. Ni J, Takehara M, Watanabe H (2010) Identification of activity related amino acid mutations of a GH9 termite cellulase. Bioresour Technol 101:6438–6443PubMedCrossRefGoogle Scholar
  140. Nimchua T, Thongaram T, Uengwetwanit T, Pongpattanakitshote S, Eurwilaichitr L (2012) Metagenomic analysis of novel lignocellulose-degrading enzymes from higher termite guts inhabiting microbes. J Microbiol Biotechnol 22:462–469PubMedCrossRefGoogle Scholar
  141. Nishida Y, Suzuki K, Kumagai Y, Tanaka H, Inoue A, Ojima T (2007) Isolation and primary structure of a cellulase from the Japanese sea urchin Strongylocentrotus nudus. Biochimie 89:1002–1011PubMedCrossRefGoogle Scholar
  142. Noda S, Ohkuma M, Yamada A, Hongoh Y, Kudo T (2003) Phylogenetic position and in situ identification of ectosymbiotic spirochetes on protists in the termite gut. Appl Environ Microbiol 69:625–633PubMedCrossRefGoogle Scholar
  143. O'Brien GW, Slaytor M (1982) Role of microorganisms in the metabolism of termites. Aust J Biol Sci 35:239–262Google Scholar
  144. O'Brien GW, Veivers PC, McEwen SE, Slaytor M, O'Brien RW (1979) The origin and distribution of cellulase in the termites Nasutitermes exitiosus and Coptotermes lacteus. Insect Biochem 9:619–625CrossRefGoogle Scholar
  145. Odelson DA, Breznak JA (1983) Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol 45:1602–1613PubMedGoogle Scholar
  146. Odelson DA, Breznak JA (1985a) Nutrition and growth characteristics of Trichomitopsis termopsidis, a cellulolytic protozoan from termites. Appl Environ Microbiol 49:614–621PubMedGoogle Scholar
  147. Odelson DA, Breznak JA (1985b) Cellulase and other polymer-hydrolysing activities of Trichomitopsis termopsidis, a symbiotic protozoan from termites. Appl Environ Microbiol 49:622–626PubMedGoogle Scholar
  148. Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61:1–9PubMedGoogle Scholar
  149. Ohkuma M, Kudo T (1996) Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl Environ Microbiol 62:461–468Google Scholar
  150. Ohkuma M, Ohtoko K, Grunau C, Moriya S, Kudo T (1998) Phylogenetic identification of the symbiotic hypermastigote Trichonympha agilis in the hindgut of the termite Reticulitermes speratus based on small-subunit rRNA sequence. J Eukaryot Microbiol 45:439–444PubMedCrossRefGoogle Scholar
  151. Ohkuma M, Iida T, Kudo T (1999a) Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites. FEMS Microbiol Lett 181:123–129PubMedCrossRefGoogle Scholar
  152. Ohkuma M, Noda S, Kudo T (1999b) Phylogeny of symbiotic methanogenes in diverse termites. FEMS Microbiol Lett 171:147–153PubMedCrossRefGoogle Scholar
  153. Ohkuma M, Ohtoko K, Iida T, Tokura M, Moriya S, Usami R, Horikoshi K, Kudo T (2000) Phylogenetic identification of hypermastigote, Pseudotrichonympha, Spirotrichonympha, Holomastigotoides, and parabasalian symbionts in the hindgut of termites. J Eukaryot Microbiol 47:249–259PubMedCrossRefGoogle Scholar
  154. Ohkuma M, Hongoh Y, Kudo T (2006) Diversity and molecular analyses of yet uncultivated microorganisms. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Heidelberg, pp 303–317CrossRefGoogle Scholar
  155. 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 4:343–349PubMedCrossRefGoogle Scholar
  156. Okada G (1975) Enzymatic studies on a cellulase system of Trichoderma viride. II. Purification and properties of two cellulases. J Biochem 77:33–42PubMedGoogle Scholar
  157. Okada G (1976) Enzymatic studies on a cellulase system of Trichoderma viride. IV. Purification and properties of a less-random type cellulase. J Biochem 80:913–922Google Scholar
  158. Oppert C, Klingeman WE, Willis JD, Oppert B, Jurat-Fuentes JL (2010) Prospecting for cellulolytic activity in insect digestive fluids. Comp Biochem Physiol B Biochem Mol Biol 155:145–154PubMedCrossRefGoogle Scholar
  159. Paster BJ, Dewhirst FE, Cooke SM, Fussing V, Poulsen LK, Breznak JA (1996) Phylogeny of not-yet-cultured spirochetes from termite guts. Appl Environ Microbiol 62:347–352PubMedGoogle Scholar
  160. Pasti MB, Belli ML (1985) Cellulolytic activity of actinomycetes isolated from termites (Termitidae) gut. FEMS Microbiol Lett 26:107–112CrossRefGoogle Scholar
  161. Paul J, Sarkar A, Varma AK (1986) In vitro studies of cellulose digesting properties of Staphylococcus saprophyticus isolated from termite gut. Curr Sci 55:710–714Google Scholar
  162. Paul J, Saxena S, Varma A (1993) Ultrastructural studies of the termite (Odontotermes obesus) gut microflora and its cellulolytic properties. World J Microbiol Biotechnol 9:108–112CrossRefGoogle Scholar
  163. Prillinger H, König H (2006) The intestinal yeasts. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Heidelberg, pp 319–334CrossRefGoogle Scholar
  164. Prillinger H, Messner R, König H, Bauer R, Lopandic K, Molnar O, Dangel P, Weigang F, Kirisitis T, Nakase T, Sigler L (1996) Yeast associated with termites: a phenotypic and genotypic characterization and use of coevolution for dating evolutionary radiations in asco- and basidiomycetes. Syst Appl Microbiol 19:265–283CrossRefGoogle Scholar
  165. Radek R, Hausmann K (1993) Symbiontische Flagellaten im Termitendarm. In: Hausmann K, Kremer BP (eds) Extremophile Mikroorganismen in ausgefallenen Lebensräumen. VCH, Weinheim, pp 325–339Google Scholar
  166. Radek R, Tischendorf G (1999) Bacterial adhesion to different termite flagellates: ultrastructural and functional evidence for distinct molecular attachment modes. Protoplasma 207:43–53CrossRefGoogle Scholar
  167. Radek R, Hausmann K, Breunig A (1992) Ectobiotic and endocytobiotic bacteria associated with the termite flagellate Joenia annectens. Acta Protozool 31:93–107Google Scholar
  168. Radek R, Roesel J, Hausmann K (1996) Light and electron microscopic study of the bacterial adhesion to termite flagellates applying lectin cytochemistry. Protoplasma 193:105–122CrossRefGoogle Scholar
  169. Rajagopal S, Rao DR, Varma AK (1979) Association of fungi in the termite gut. Curr Sci 48:998–999Google Scholar
  170. Rajagopal S, Rao DR, Varma AK (1981) Fungi from worker termite gut, Odontotermes obesus (Rambur) from northern India. Nova Hedwig 34:97–100Google Scholar
  171. Reuss J, König H, Dröge S (2013) Isolation of methanotrophic bacteria from termite gut. Biospektrum. Annual Conference of the Association for General and Applied Microbiology. Special issue, p 96Google Scholar
  172. Rouland C, Civas A, Renoux J, Petek F (1988) Purification and properties of cellulases from the termite Macrotermes mülleri (Termitidae, Macrotermitinae) and its symbiotic fungus Termitomyces sp. Comp Biochem Physiol 91B:449–458Google Scholar
  173. Rouland C, Lenoir F, Lepage M (1991) The role of the symbiotic fungus in the digestive metabolism of several species of fungus-growing termites. Comp Biochem Physiol 99A:657–663CrossRefGoogle Scholar
  174. Rouland C, Braumann A, Labat M, Lapage M (1993) Nutritional factors affecting methane emission from termites. Chemosphere 26:617–622CrossRefGoogle Scholar
  175. Sanderson MG (1996) Biomass of termites and their emissions of methane and carbon dioxide: a global database. Global Biochem Cycles 10:543–557CrossRefGoogle Scholar
  176. Saxena S, Bahadur J, Varma A (1993) Cellulose and hemicellulose degrading bacteria from the termite gut and mound soils of India. Indian J Microbiol 33:55–60Google Scholar
  177. 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 80:471–478PubMedCrossRefGoogle Scholar
  178. Scharf ME, Wu-Scharf D, Pittendrigh BR, Bennett GW (2003) Caste- and development-associated gene expression in a lower termite. Genome Biol 4:R62PubMedCrossRefGoogle Scholar
  179. Scharf ME, Karl ZJ, Sethi A, Boucias DG (2011) Multiple levels of synergistic collaboration in termite lignocellulose digestion. PLoS One 6:e21709. doi: 10.1371/journal.pone.0021709 PubMedCrossRefGoogle Scholar
  180. 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
  181. Schulein M, Tikhomirou DF, Schou C (1993) Humicola insolens alkaline cellulases. Found Biotechnol Ind Ferment Res 8:109–116Google Scholar
  182. Schultz JE, Breznak JA (1978) Heterotrophic bacteria present in hindgut of wood-eating termites [Reticulitermes flavipes (Kollar)]. Appl Environ Microbiol 35:930–936PubMedGoogle Scholar
  183. Schulz MW, Slaytor M, Hogan ME, O'Brien RW (1986) Components of the cellulase from the higher termite, Nasutitermes walkeri. Insect Biochem 16:929–932CrossRefGoogle Scholar
  184. Scrivener AM, Slaytor M (1994) Properties of the endogenous cellulase from Panesthia cribrata Saussure and purification of major endo-β-1,4-glucanase components. Insect Biochem Mol Biol 24:223–231CrossRefGoogle Scholar
  185. Sebald M, Prévot AR (1962) Étude d'une nouvelle espèce anaérobic stricte Micromonospora acetoformici n. sp. isolée de l’intestin postérieur de Reticulitermes lucifugus var. santonensis. Ann Inst Pasteur Paris 102:199–214Google Scholar
  186. Seifert K, Becker G (1965) Der chemische Abbau von Laub- und Nadelholzarten durch verschiedene Termiten. Holzforschung 19:105–111Google Scholar
  187. Seiler W, Conrad R, Scharffe D (1984) Field studies of methane emission from termite nests into the atmosphere and measurement of methane uptake by tropical soils. J Atmos Chem 1:171–186CrossRefGoogle Scholar
  188. Shimada K, Maekawa K (2010) Changes in endogenous cellulase gene expression levels and reproductive characteristics of primary and secondary reproductives with colony development of the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). J Insect Physiol 56:1118–1124Google Scholar
  189. Sillam-Dussès D, Krasulová J, Vrkoslav V, Pytelková J, Cvačka J, Kutalová K, Bourguignon T, Miura T, Šobotník J (2012) Comparative study of the labial gland secretion in termites (Isoptera). PLoS One 7:e46431. doi: 10.1371/journal.pone.0046431 PubMedCrossRefGoogle Scholar
  190. Slaytor M (1992) Cellulose digestion in termites and cockroaches: what role do symbionts play? Comp Biochem Physiol 103B:775–784Google Scholar
  191. Smant G, Stokkermans JPWG, Yan YT, de Boer JM, Baum TJ, Wang XH, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of β-1,4-glucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci U S A 95:4096–4911CrossRefGoogle Scholar
  192. Snyder TE (1949) Catalog of the termites (Isoptera) of the world. Smithson Misc Coll 112:1–490Google Scholar
  193. Stark JR, Walker RS (1983) Carbohydrate digestion in Pecten maximus. Comp Biochem Physiol 76B:173–177Google Scholar
  194. Suzuki K, Ojima IT, Nishita K (2003) Purification and cDNA cloning of a cellulase from abalone Haliotis discus hannai. Eur J Biochem 270:771–778PubMedCrossRefGoogle Scholar
  195. Taechapoempol K, Sreethawong T, Rangsunvigit P, Namprohm W, Thamprajamchit B, Rengpipat S, Chavadej S (2011) Cellulase-producing bacteria from Thai higher termites, Microcerotermes sp.: enzymatic activities and ionic liquid tolerance. Appl Biochem Biotechnol 164:204–219PubMedCrossRefGoogle Scholar
  196. Takashima S, Iikura H, Nakamura A, Hidaka M, Masaki H, Uozumi T (1999) Comparison of gene structures and enzymatic properties between two endoglucanases from Humicola grisea. J Biotechnol 67:85–97PubMedCrossRefGoogle Scholar
  197. Tanaka H, Aoyagi H, Shiina S, Doudou Y, Yoshimura T, Nakamura R, Uchiyama H (2006) Influence of the diet components on the symbiotic microorganisms community in hindgut of Coptotermes formosanus Shiraki. Appl Microbiol Biotechnol 71:907–917PubMedCrossRefGoogle Scholar
  198. Thayer DW (1976) Facultative wood-digesting bacteria from the hindgut of the termite Reticulitermes hesperus. J Gen Microbiol 95:287–296CrossRefGoogle Scholar
  199. Thayer DW (1978) Carboxymethylcellulase produced by facultative bacteria from the hind-gut of the termite Reticulitermes hesperus. J Gen Microbiol 106:13–18PubMedCrossRefGoogle Scholar
  200. 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 Microb 65:4497–4505Google Scholar
  201. 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
  202. To LP, Margulis L, Chase D, Nutting WL (1980) The symbiotic microbial community of the sonoran desert termite: Pterotermes occidentis. Biosystems 13:109–137PubMedCrossRefGoogle Scholar
  203. Todaka N, Lopez CM, Inoue T, Saita K, Maruyama J, Arioka M, Kitamoto K, Kudo T, Moriya S (2010) Heterologous expression and characterization of an endoglucanase from a symbiotic protist of the lower termite, Reticulitermes speratus. Appl Biochem Biotechnol 160:1168–1178PubMedCrossRefGoogle Scholar
  204. Todaka N, Nakamura R, Moriya S, Ohkuma M, Kudo T, Takahashi H, Ishida N (2011) Screening of optimal cellulases from symbiotic protists of termites through expression in the secretory pathway of Saccharomyces cerevisiae. Biosci Biotechnol Biochem 75:2260–2263PubMedCrossRefGoogle Scholar
  205. Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339PubMedCrossRefGoogle Scholar
  206. Tokuda G, Watanabe H, Matsumoto T, Noda H (1997) Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): distribution of cellulases and properties of endo-beta-1,4-glucanase. Zool Sci 14:83–93PubMedCrossRefGoogle Scholar
  207. 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 1447:146–159PubMedCrossRefGoogle Scholar
  208. Tokuda G, Yamaoka I, Noda H (2000) Localization of symbiotic clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki). Appl Environ Microb 66:2199–2207CrossRefGoogle Scholar
  209. Tokuda G, Lo N, Watanabe H, Arakawa G, Matsumoto T, Noda H (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol Ecol 13:3219–3228PubMedCrossRefGoogle Scholar
  210. 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
  211. Tokuda G, Watanabe H, Hojo M, Fujita A, Makiya H, Miyagi M, Arakawa G, Arioka M (2012) Cellulolytic environment in the midgut of the wood-feeding higher termite Nasutitermes takasagoensis. J Insect Physiol 58:147–154PubMedCrossRefGoogle Scholar
  212. 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 33:233–240PubMedCrossRefGoogle Scholar
  213. Tomme P, Warren RAJ, Gilkes NR (1995) Cellulose hydrolysis by bacteria and fungi. Adv Microb Physiol 37:1–81PubMedCrossRefGoogle Scholar
  214. Tracey MV, Youatt G (1958) Cellulase and chitinase in two species of Australian termites. Enzymologia 19:70–72PubMedGoogle Scholar
  215. Trager W (1932) A cellulase from the symbiotic intestinal flagellates of termites and of the roach, Cryptocercus punctulatus. Biochem J 26:1762–1771PubMedGoogle Scholar
  216. Trinkerl M, Breunig A, Schauder R, König H (1990) Desulfovibrio termitidis sp. nov., a carbohydrate-degrading sulfate-reducing bacterium from the hindgut of a termite. Syst Appl Microbiol 13:373–377CrossRefGoogle Scholar
  217. Tsuji A, Sato S, Kondo A, Tominaga K, Yuasa K (2012) Purification and characterization of cellulase from North Pacific krill (Euphausia pacifica). Analysis of cleavage specificity of the enzyme. Comp Biochem Physiol B Biochem Mol Biol 163:324–333PubMedCrossRefGoogle Scholar
  218. 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 15:9–28CrossRefGoogle Scholar
  219. Veivers PC, Musca AM, O'Brien RW, Slaytor M (1982) Digestive enzymes of the salivary glands and gut of Mastotermes darwiniensis. Insect Biochem 12:35–40CrossRefGoogle Scholar
  220. Veivers PC, O'Brien RW, Slaytor M (1983) Selective defaunation of Mastotermes darwiniensis and its effect on cellulose and starch metabolism. Insect Biochem 13:95–101CrossRefGoogle Scholar
  221. Veivers PC, Mühlemann R, Slaytor M, Leuthold RH, Bignell DE (1991) Digestion, diet and polyethism in two fungus-growing termites: Macrotermes subhyalinus Rambur and M. michaelseni Sjøstedt. J Insect Physiol 37:675–682CrossRefGoogle Scholar
  222. Viscogliosi E, Philippe H, Baroin A, Perasso R, Brugerolle G (1993) Phylogeny of trichomonads based on partial sequences of large subunit rRNA and on cladistic analysis of morphological data. J Eukyot Microbiol 40:411–421CrossRefGoogle Scholar
  223. Wang ZY, Hu TT, Liu J, Lu YJ, Mo JC (2011a) Artificial culture and domestication of Termitomyces fungi in China. Sociobiology 57:675–686Google Scholar
  224. Wang ZY, Lu YJ, Mao GQ, Mo JC (2011b) Review on the research of Termitomyces taxonomy in China. Sociobiology 57:597–605Google Scholar
  225. Wang ZY, Mao GQ, Lu YJ, Mo JC (2011c) Biology and ecology of Termitomyces fungus in China. Sociobiology 57:621–631Google Scholar
  226. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernández M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedCrossRefGoogle Scholar
  227. Watanabe H, Tokuda G (2001) Animal cellulases. Cell Mol Life Sci 58:1167–1178PubMedCrossRefGoogle Scholar
  228. Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632PubMedCrossRefGoogle Scholar
  229. Watanabe H, Nakamura M, Tokuda G, Yamaoka I, Scrivener AM, Noda H (1997) Site of secretion and properties of endogenous endo-beta-1,4-glucanase components from Reticulitermes speratus (Kolbe), a Japanese subterranean termite. Insect Biochem Mol Biol 27:305–313PubMedCrossRefGoogle Scholar
  230. Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331PubMedCrossRefGoogle Scholar
  231. 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
  232. Watanabe Y, Shinzato N, Fukatsu T (2003) Isolation of actinomycetes from termites' guts. Biosci Biotechnol Biochem 67:1797–1801PubMedCrossRefGoogle Scholar
  233. Watanabe H, Takase A, Tokuda G, Yamada A, Lo N (2006) Symbiotic “Archaezoa” of the primitive termite Mastotermes darwiniensis still play a role in cellulase production. Eukaryot Cell 5:1571–1576PubMedCrossRefGoogle Scholar
  234. 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 92:32–40PubMedCrossRefGoogle Scholar
  235. Wenzel M, Radek R, Brugerolle G, König H (2003) Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. Eur J Protistol 39:11–23CrossRefGoogle Scholar
  236. Wheeler MM, Zhou X, Scharf ME, Oi FM (2007) Molecular and biochemical markers for monitoring dynamic shifts of cellulolytic protozoa in Reticulitermes flavipes. Insect Biochem Mol Biol 37:1366–1374PubMedCrossRefGoogle Scholar
  237. Wier A, Dolan M, Grimaldi D, Guerrero R, Wagensberg J, Margulis L (2002) Spirochete and protist symbionts of a termite (Mastotermes electrodominicus) in Miocene amber. Proc Natl Acad Sci U S A 99:1410–1413PubMedCrossRefGoogle Scholar
  238. Willis JD, Oppert B, Oppert C, Klingeman WE, Jurat-Fuentes JL (2011) Identification, cloning, and expression of a GHF9 cellulase from Tribolium castaneum (Coleoptera: Tenebrionidae). J Insect Physiol 57:300–306PubMedCrossRefGoogle Scholar
  239. Wood TG, Sands WA (1978) The role of termites in ecosystems. In: Brian JV (ed) Production ecology of ants and termites. Cambridge University Press, Cambridge, pp 245–292Google Scholar
  240. Xu BZ, Hellman U, Ersson B, Janson JC (2000) Purification, characterization and amino-acid sequence analysis of a thermostable, low molecular mass endo-β-1,4-glucanase from the blue mussel, Mytilus edulis. Eur J Biochem 267:4970–4977PubMedCrossRefGoogle Scholar
  241. Xu BZ, Janson JC, Sellos D (2001) Cloning and sequencing of a molluscan endo-β-1,4-glucanase gene from the blue mussel, Mytilus edulis. Eur J Biochem 268:3718–3727PubMedCrossRefGoogle Scholar
  242. Yamaoka J, Nagatani Y (1975) Cellulose digestion system in the termite, Reticulitermes speratus (Kolbe). I. Producing sites and physiological significance of two kinds of cellulase in the worker. Zool Mag 84:23–29Google Scholar
  243. Yamin MA (1978) Axenic cultivation of the cellulolytic flagellate Trichomitopsis termopsidis (Cleveland) from the termite Zootermopsis. J Protozool 25:535–538Google Scholar
  244. Yamin MA (1979) Flagellates of the orders Trichomondida Kirby, Oxymonadida Grassé, and Hypermastigida Grassi & Foà reported from lower termites (Isoptera families Mastotermitidae, Kalotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae, and Serritermitidae) and from the wood-feeding roach Cryptocercus (Dictyoptera: Cryptocercidae). Sociobiology 4:4–119Google Scholar
  245. Yamin MA (1980) Cellulose metabolism by the termite flagellate Trichomitopsis termopsidis. Appl Environ Microbiol 39:859–863PubMedGoogle Scholar
  246. Yamin MA (1981) Cellulose metabolism by the flagellate Trichonympha from the termite is independent of endosymbiotic bacteria. Science 211:58–59PubMedCrossRefGoogle Scholar
  247. Yang F, Xu B, Li J, Huang Z (2012) Transcriptome analysis of Termitomyces albuminosus reveals the biodegradation of lignocellulose. Wei Sheng Wu Xue Bao 52:466–477PubMedGoogle Scholar
  248. Yokoe Y (1964) Cellulase activity in the termite, Leucotermes speratus, with new evidence in support of a cellulase produced by the termite itself. Sci Paper Coll Gen Educ Univ Tokyo 14:115–120Google Scholar
  249. Yokoe Y, Yasumasu I (1964) The distribution of cellulase in invertebrates. Comp Biochem Physiol 13:323–338PubMedCrossRefGoogle Scholar
  250. Yoshigi N, Taniguch H, Sasaki T (1988) Purification and properties of a new endo-cellulase from Robillarda sp. Y-20. Agric Biol Chem 52:1389–1396CrossRefGoogle Scholar
  251. Yoshimura T, Tsunoda K, Takahashi M (1996) Degradation of wood in the digestive tract of a higher termite, Nasutitermes takasagoensis (Shiraki) (Isoptera: Termitidae). Mokuzai Gakkaishi 42:1250–1257Google Scholar
  252. Yuki M, Moriya S, Inoue T, Kudo T (2008) Transcriptome analysis of the digestive organs of H. sjostedti, a lower termite that hosts mutualistic microorganisms in its hindgut. Zool Sci 25:401–406PubMedCrossRefGoogle Scholar
  253. Zhang D, Lax AR, Raina AK, Bland JM (2009) Differential cellulolytic activity of native-form and C-terminal tagged-form cellulase derived from Coptotermes formosanus and expressed in E. coli. Insect Biochem Mol Biol 39:516–522PubMedCrossRefGoogle Scholar
  254. Zhang D, Lax AR, Bland JM, Allen AB (2011) Characterization of a new endogenous endo-β-1,4-glucanase of Formosan subterranean termite (Coptotermes formosanus). Insect Biochem Mol Biol 41:211–218PubMedCrossRefGoogle Scholar
  255. Zhou X, Smith JA, Oi FM, Koehler PG, Bennett GW, Scharf ME (2007) Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 395:29–39PubMedCrossRefGoogle Scholar
  256. Zhou X, Wheeler MM, Oi FM, Scharf ME (2008) RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochem Mol Biol 38:805–815PubMedCrossRefGoogle Scholar
  257. Zhou X, Kovaleva ES, Wu-Scharf D, Campbell JH, Buchman GW, Boucias DG, Scharf ME (2010) Production and characterization of a recombinant beta-1,4-endoglucanase (glycohydrolase family 9) from the termite Reticulitermes flavipes. Arch Insect Biochem Physiol 74:147–162PubMedCrossRefGoogle Scholar
  258. Zimmer M, Topp W (1998) Microorganisms and cellulose digestion in the gut of the woodlouse Porcellio scaber. J Chem Ecol 24:1397–1408CrossRefGoogle Scholar
  259. 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-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Institute of Microbiology and Wine ResearchJohannes Gutenberg University of MainzMainzGermany

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