Methanogenesis in the Digestive Tracts of Insects and Other Arthropods

  • Andreas BruneEmail author
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Termites, cockroaches, and scarab beetle larvae are the only insects known to emit methane, but they do so in impressive amounts. Methanogenesis occurs in the enlarged hindgut compartment and is fueled by hydrogen and reduced one-carbon compounds formed during symbiotic digestion of plant fiber and humus. The methanogens either colonize the hindgut wall or are associated with symbiotic protists. They comprise only a relatively small number of lineages from four methanogenic orders that are restricted to the intestinal tract of insects and millipedes. The host specificity of most lineages and the metabolic properties of the few isolates available to date indicate that they are well adapted to the microenvironment of their intestinal habitats. Methanogenesis is generally expected to stimulate symbiotic digestion, but benefits for the host are not well documented. Although the methane emissions of termites are mitigated by the methanotrophic activity of their mounds and the surrounding soil, their enormous biomass in the tropics makes them a significant natural source of atmospheric methane at the global scale.


  1. Akhmanova A, Voncken FGJ, van Alen T, van Hoek A, Boxma B, Vogels G, Veenhuis M, Hackstein JHP (1998) A hydrogenosome with a genome. Nature 396:527–528PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bauer E, Lampert N, Mikaelyan A, Köhler T, Maekawa K, Brune A (2015) Physicochemical conditions, metabolites, and community structure of the bacterial microbiota in the gut of wood-feeding cockroaches (Blaberidae: Panesthiinae). FEMS Microbiol Ecol 91:1–14PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bayon C (1980) Volatile fatty acids and methane production in relation to anaerobic carbohydrate fermentation in Oryctes nasicornis larvae (Coleoptera: Scarabaeidae). J Insect Physiol 26:819–828CrossRefGoogle Scholar
  4. Bayon C, Etiévant P (1980) Methanic fermentation in the digestive tract of a xylophageous insect: Oryctes nasicorni L. larva (Coleoptera; Scarabaeidae). Experientia 36:154–155CrossRefGoogle Scholar
  5. Bignell DE (1984a) Direct potentiometric determination of redox potentials of the gut contents in the termites Zootermopsis nevadensis and Cubitermes severus and in three other arthropods. J Insect Physiol 30:169–174CrossRefGoogle Scholar
  6. Bignell DE (1984b) The arthropod gut as an environment for microorganisms. In: Anderson JM, Rayner ADM, Walton DWH (eds) Invertebrate–microbial interactions. Cambridge University Press, Cambridge, England, pp 205–227Google Scholar
  7. Bignell DE (2010) Termites. In: Reay D, Smith P, van Amstel A (eds) Methane and climate change. Earthscan, London, pp 62–73Google Scholar
  8. Bignell DE, Oskarsson H, Anderson JM (1980) Specialization of the hindgut wall for the attachment of symbiotic microorganisms in a termite Procubitermes aburiensis. Zoomorphology 96:103–112CrossRefGoogle Scholar
  9. Bignell DE, Eggleton P, Nunes L, Thomas KL (1997) Termites as mediators of carbon fluxes in tropical forests: budgets for carbon dioxide and methane emissions. In: Watt AB, Stork NE, Hunter MD (eds) Forests and insects. Chapman & Hall, London, pp 109–134Google Scholar
  10. Bijnen FGC, Harren FJM, Hackstein JHP, Reuss J (1996) Intracavity CO laser photoacoustic trace gas detection: cyclic CH4, H2O and CO2 emission by cockroaches and scarab beetles. Appl Opt 35:5357–5368PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bond JH Jr, Engel RR, Levitt MD (1971) Factors influencing pulmonary methane excretion in man: an indirect method of studying the in situ metabolism of the methane-producing colonic bacteria. J Exp Med 133:572–588PubMedPubMedCentralCrossRefGoogle Scholar
  12. Borken W, Grundel S, Beese F (2000) Potential contribution of Lumbricus terrestris L. to carbon dioxide, methane and nitrous oxide fluxes from a forest soil. Biol Fertil Soils 32:142–148CrossRefGoogle Scholar
  13. Borrel G, Harris HMB, Tottey W, Mihajlosvki A, Parisot N, Peyretaillade E, Peyret P, Gribaldo S, O'Toole PW, Brugère J-F (2012) Genome sequence of “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 194:6944–6945PubMedPubMedCentralCrossRefGoogle Scholar
  14. Boucias DG, Cai Y, Sun Y, Lietze V-U, Sen R, Raychoudhury R, Scharf ME (2013) The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its responses to dietary lignocellulose composition. Mol Ecol 22:1836–1853PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bourguignon T, Lo N, Dietrich C, Šobotník J, Sidek S, Roisin Y, Brune A, Evans TA (2018) Rampant host-switching shaped the termite gut microbiome. Curr Biol 28:649–654.e2PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bracke JW, Loeb Cruden D, Markovetz AJ (1978) Effect of metronidazole on the intestinal microflora of the American cockroach, Periplaneta americana L. Antimicrob Agents Chemother 13:115–120PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brauman A, Kane M, Breznak JA (1992) Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384–1387PubMedPubMedCentralCrossRefGoogle Scholar
  18. Brauman A, Dore J, Eggleton P, Bignell D, Breznak JA, Kane MD (2001) Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol Ecol 35:27–36PubMedPubMedCentralCrossRefGoogle Scholar
  19. Breznak JA (1975) Symbiotic relationships between termites and their intestinal microbiota. Symp Soc Exp Biol 29:559–580Google Scholar
  20. 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 209–231CrossRefGoogle Scholar
  21. Breznak JA, Switzer JM (1986) Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl Environ Microbiol 52:623–630PubMedPubMedCentralGoogle Scholar
  22. Breznak JA, Brill WJ, Mertins JW, Coppel HC (1973) Nitrogen fixation in termites. Nature 244:577–580PubMedPubMedCentralCrossRefGoogle Scholar
  23. Breznak JA, Mertins JW, Coppel HC (1974) Nitrogen fixation and methane production in a wood-eating cockroach, Cryptocercus punctulatus Scudder (Orthoptera: Blattidae). Univ Wisc Forest Res Notes 184:1–2Google Scholar
  24. Brune A (2010a) Methanogens in the digestive tract of termites. In: Hackstein JHP (ed) (Endo)symbiotic methanogenic archaea. Springer, Heidelberg, pp 81–100CrossRefGoogle Scholar
  25. Brune A (2010b) Methanogenesis in the digestive tracts of insects. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol 8. Springer, Heidelberg, pp 707–728CrossRefGoogle Scholar
  26. Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12:168–180PubMedPubMedCentralCrossRefGoogle Scholar
  27. Brune A, Kühl M (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42:1121–1127CrossRefGoogle Scholar
  28. Brune A, Ohkuma M (2011) Role of the termite gut microbiota in symbiotic digestion. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 439–475Google Scholar
  29. Brune A, Frenzel P, Cypionka H (2000) Life at the oxic–anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24:691–710PubMedPubMedCentralCrossRefGoogle Scholar
  30. Byzov BA (2006) Intestinal microbiota of millipedes. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 89–114CrossRefGoogle Scholar
  31. Cao Y, Sun J-Z, Rodriguez JM, Lee KC (2010) Hydrogen emission by three wood-feeding subterranean termite species (Isoptera: Rhinotermitidae): production and characteristics. Ins Sci 17:237–244CrossRefGoogle Scholar
  32. Ceja-Navarro JA, Nguyen NH, Karaoz U, Gross SR, Herman DJ, Andersen GL, Bruns TD, Pett-Ridge J, Blackwell M, Brodie EL (2014) Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. ISME J 8:6–18PubMedPubMedCentralCrossRefGoogle Scholar
  33. Collins NM, Wood TG (1984) Termites and atmospheric gas production. Science 224:84–86PubMedPubMedCentralCrossRefGoogle Scholar
  34. Cook SF (1932) The respiratory gas exchange in Termopsis nevadensis. Biol Bull 63:246–257CrossRefGoogle Scholar
  35. Darlington JPEC, Zimmerman PR, Greenberg J, Westberg C, Bakwin P (1997) Production of metabolic gases by nests of the termite Macrotermes jeanneli in Kenya. J Trop Ecol 13:491–510CrossRefGoogle Scholar
  36. de Angelis MA, Lee C (1994) Methane production during zooplankton grazing on marine phytoplankton. Limnol Oceanogr 39:1298–1308CrossRefGoogle Scholar
  37. Deevong P, Hattori S, Yamada A, Trakulnaleamsai S, Ohkuma M, Noparatnaraporn N, Kudo T (2004) Isolation and detection of methanogens from the gut of higher termites. Microb Environ 19:221–226CrossRefGoogle Scholar
  38. Delmas RA, Servant J, Tathy JP, Cros B, Labat M (1992) Sources and sinks of methane and carbon dioxide exchanges in mountain forest in equatorial Africa. J Geophys Res 97D:6169–6179CrossRefGoogle Scholar
  39. Denman KL, Brasseur G, Chidthaisong A, Ciais P, Cox PM et al (2007) Couplings between changes in the climate system and biogeochemistry. In: Solomon S et al (eds) Climate change 2007: the physical science basis. Fourth assessment report of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University Press, Cambridge, pp 499–587Google Scholar
  40. Depkat-Jakob PS, Hunger S, Schulz K, Brown GG, Tsai SM, Drake HL (2012) Emission of methane by Eudrilus eugeniae and other earthworms from Brazil. Appl Environ Microbiol 78:3014–3019PubMedPubMedCentralCrossRefGoogle Scholar
  41. Desai MS, Brune A (2012) Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. ISME J 6:1302–1313PubMedPubMedCentralCrossRefGoogle Scholar
  42. Ditchfield AK, Wilson ST, Hart MC, Purdy KJ, Green DH, Hatton AD (2012) Identification of putative methylotrophic and hydrogenotrophic methanogens within sedimenting material and copepod faecal pellets. Aquat Microb Ecol 67:151–160CrossRefGoogle Scholar
  43. Doddema HJ, Vogels GD (1978) Improved identification of methanogenic bacteria by fluorescence microscopy. Appl Environ Microbiol 36:752–754PubMedPubMedCentralGoogle Scholar
  44. Donovan SE, Purdy KJ, Kane MD, Eggleton P (2004) Comparison of Euryarchaea strains in the guts and food-soil of the soil-feeding termite Cubitermes fungifaber across different soil types. Appl Environ Microbiol 70:3884–3892PubMedPubMedCentralCrossRefGoogle Scholar
  45. Drake HL, Horn MA (2007) As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annu Rev Microbiol 61:169–189PubMedPubMedCentralCrossRefGoogle Scholar
  46. Dridi B, Fardeau M-L, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62:1902–1907PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 63:4039–4046PubMedPubMedCentralGoogle Scholar
  48. Egert M, Wagner B, Lemke T, Brune A, Friedrich MW (2003) Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microbiol 69:6659–6668PubMedPubMedCentralCrossRefGoogle Scholar
  49. Egert M, Stingl U, Dyhrberg Bruun L, Wagner B, Brune A, Friedrich MW (2005) Structure and topology of microbial communities in the major gut compartments of Melolontha melolontha larvae (Coleoptera: Scarabaeidae). Appl Environ Microbiol 71:4556–4566PubMedPubMedCentralCrossRefGoogle Scholar
  50. Eggleton P, Homathevi R, Jones DT, MacDonald JA, Jeeva D, Bignell DE, Davies RG, Maryati M (1999) Termite assemblages, forest disturbance and greenhouse gas fluxes in Sabah, East Malaysia. Phil Trans R Soc Lond B 354:1791–1802CrossRefGoogle Scholar
  51. Fenchel T, Finlay BJ (1992) Production of methane and hydrogen by anaerobic ciliates containing symbiotic methanogens. Arch Microbiol 157:475–480Google Scholar
  52. Finlay BJ, Esteban G, Clarke KJ, Williams AG, Embley TM, Hirt RP (1994) Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiol Lett 117:157–161PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 67:4880–4890PubMedPubMedCentralCrossRefGoogle Scholar
  54. Gijzen HJ, Barugahare M (1992) Contribution of anaerobic protozoa and methanogens to hindgut metabolic activities of the American cockroach, Periplaneta americana. Appl Environ Microbiol 58:2565–2570PubMedPubMedCentralGoogle Scholar
  55. Gijzen HJ, Broers CA, Barugahare M, Stumm CK (1991) Methanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalis in the cockroach hindgut. Appl Environ Microbiol 57:1630–1634PubMedPubMedCentralGoogle Scholar
  56. Gilmour D (1940) The anaerobic gaseous metabolism of the roach, Cryptocercus punctulatus scudder. Biol Bull 79:297–308CrossRefGoogle Scholar
  57. Hackstein JHP (2010) Anaerobic ciliates and their methanogenic endosymbionts. In: JHP H (ed) (Endo)symbiotic Methanogenic Archaea. Springer, Heidelberg, pp 13–23CrossRefGoogle Scholar
  58. Hackstein JHP, Stumm CK (1994) Methane production in terrestrial arthropods. Proc Natl Acad Sci USA 91:5441–5445PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hackstein JHP, van Alen TA (2010) Methanogens in the gastro-intestinal tract of animals. In: Hackstein JHP (ed) (Endo)symbiotic methanogenic archaea. Springer, Heidelberg, pp 115–142CrossRefGoogle Scholar
  60. Hackstein JHP, van Alen TA, Rosenberg J (2006) Methane production by terrestrial arthropods. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Berlin, pp 155–180CrossRefGoogle Scholar
  61. Hara K, Shinzato N, Seo M, Oshima T, Yamagishi A (2002) Phylogenetic analysis of symbiotic archaea living in the gut of xylophagous cockroaches. Microb Environ 17:185–190CrossRefGoogle Scholar
  62. Hara K, Shinzato N, Oshima T, Yamagishi A (2004) Endosymbiotic Methanobrevibacter species living in symbiotic protists of the termite Reticulitermes speratus detected by fluorescent in situ hybridization. Microb Environ 19:120–127CrossRefGoogle Scholar
  63. Ho A, Erens H, Mujinya BB, Boeckx P, Baert G, Schneider B, Frenzel P, Boon N, Van Ranst E (2013) Termites facilitate methane oxidation and shape the methanotrophic community. Appl Environ Microbiol 79:7234–7240PubMedPubMedCentralCrossRefGoogle Scholar
  64. Hongoh Y, Ohkuma M (2010) Termite gut flagellates and their methanogenic and eubacterial symbionts. In: Hackstein JHP (eds) (Endo)symbiotic Methanogenic Archaea. Springer, Heidelberg, pp 55–79CrossRefGoogle Scholar
  65. Horn MA, Schramm A, Drake HL (2003) The earthworm gut: an ideal habitat for ingested N2O-producing microorganisms. Appl Environ Microbiol 69:1662–1669PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hungate RE (1938) Studies on the nutrition of Zootermopsis II. The relative importance of the termite and the protozoa in wood digestion. Ecology 19:1–25CrossRefGoogle Scholar
  67. Hungate RE (1939) Experiments on the nutrition of Zootermopsis. III. The anaerobic carbohydrate dissimilation by the intestinal protozoa. Ecology 20:230–245CrossRefGoogle Scholar
  68. Hungate RE (1943) Quantitative analyses of the cellulose fermentation by termite protozoa. Ann Entomol Soc Am 36:730–739CrossRefGoogle Scholar
  69. Hungate RE (1946) The symbiotic utilization of cellulose. J Elisha Mitchell Sci Soc 62:9–24Google Scholar
  70. Hungate RE (1977) The rumen microbial ecosystem. Annu Rev Microbiol 33:1–20CrossRefGoogle Scholar
  71. Iino T, Tamaki H, Tamazawa S, Ueno Y, Ohkuma M, Suzuki K, Igarashi Y, Haruta S (2013) Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov. for a methanogenic lineage of the class Thermoplasmata. Microbes Environ 28:244–250PubMedPubMedCentralCrossRefGoogle Scholar
  72. Inoue J, Noda S, Hongoh Y, Ui S, Ohkuma M (2008) Identification of endosymbiotic methanogen and ectosymbiotic spirochetes of gut protists of the termite Coptotermes formosanus. Microb Environ 23:94–97CrossRefGoogle Scholar
  73. Jamali H, Livesley SJ, Dawes TZ, Cook GD, Hutley LB, Arndt SK (2011a) Diurnal and seasonal variations in CH4 flux from termite mounds in tropical savannas of the Northern Territory, Australia. Agric Forest Meteorol 151:1471–1479CrossRefGoogle Scholar
  74. Jamali H, Livesley SJ, Dawes TZ, Hutley LB, Arndt SK (2011b) Termite mound emissions of CH4 and CO2 are primarily determined by seasonal changes in termite biomass and behaviour. Oecologia 167:525–553PubMedPubMedCentralCrossRefGoogle Scholar
  75. Jamali H, Livesley SJ, Hutley LB, Fest B, Arndt SK (2013) The relationship between termite mound CH4/CO2 emissions and internal concentration ratios are species specific. Biogeosciences 10:2229–2240CrossRefGoogle Scholar
  76. Janssen PH, Kirs M (2008) Structure of the archaeal community of the rumen. Appl Environ Microbiol 74:3619–3625PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kammann C, Hepp S, Lenhart K, Müller C (2009) Stimulation of methane consumption by endogenous CH4 production in aerobic grassland soil. Soil Biol Biochem 41:622–629CrossRefGoogle Scholar
  78. Kane MD, Breznak JA (1991) Effect of host diet on production of organic acids and methane by cockroach gut bacteria. Appl Environ Microbiol 57:2628–2634PubMedPubMedCentralGoogle Scholar
  79. Kappler A, Brune A (2002) Dynamics of redox potential and changes in redox state of iron and humic acids during gut passage in soil-feeding termites (Cubitermes spp.). Soil Biol Biochem 34:221–227CrossRefGoogle Scholar
  80. Karl DM, Tilbrook BD (1994) Production and transport of methane in oceanic particulate organic matter. Nature 368:732–734CrossRefGoogle Scholar
  81. Khalil MAK, Rasmussen RA, French JRJ, Holt JA (1990) The influence of termites on atmospheric trace gases: CH4, CO2, CHCl3, N2O, CO, H2, and light hydrocarbons. J Geophys Res 95:3619–3634CrossRefGoogle Scholar
  82. Kinsman R, Sauer FD, Jackson HA, Wolynetz MS (1995) Methane and carbon dioxide emissions from dairy cows in full lactation monitored over a six-month period. J Dairy Sci 78:2760–2766PubMedPubMedCentralCrossRefGoogle Scholar
  83. Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG et al (2013) Three decades of global methane sources and sinks. Nat Geosci 6:813–823CrossRefGoogle Scholar
  84. 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 78:4691–4701PubMedPubMedCentralCrossRefGoogle Scholar
  85. Kumaresan D, Stralis-Pavese N, Abell GCJ, Bodrossy L, Murrell JC (2011) Physical disturbance to ecological niches created by soil structure alters community composition of methanotrophs. Environ Microbiol Rep 3:613–621PubMedPubMedCentralCrossRefGoogle Scholar
  86. Lang K, Schuldes J, Klingl A, Poehlein A, Daniel R, Brune A (2015) New mode of energy metabolism in the seventh order of methanogens as indicated by comparative genome analysis of “Candidatus Methanoplasma termitum”. Appl Environ Microbiol 81:1338–1352PubMedPubMedCentralCrossRefGoogle Scholar
  87. 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 62:3620–3631PubMedPubMedCentralGoogle Scholar
  88. Leadbetter JR, Crosby LD, Breznak JA (1998) Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch Microbiol 169:287–292PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lee MJ, Schreurs PJ, Messer AC, Zinder SH (1987) Association of methanogenic bacteria with flagellated protozoa from a termite hindgut. Curr Microbiol 15:337–341CrossRefGoogle Scholar
  90. 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 67:4657–4661PubMedPubMedCentralCrossRefGoogle Scholar
  91. Lemke T, Stingl U, Egert M, Friedrich MW, Brune A (2003) Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microbiol 69:6650–6658PubMedPubMedCentralCrossRefGoogle Scholar
  92. Lighton JRB, Ottesen EA (2005) To DGC or not to DGC: oxygen guarding in the termite Zootermopsis nevadensis (Isoptera: Termopsidae). J Exp Biol 208:4671–4678PubMedPubMedCentralCrossRefGoogle Scholar
  93. Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189PubMedPubMedCentralCrossRefGoogle Scholar
  94. MacDonald JA, Eggleton P, Bignell DE, Forzi F, Fowler D (1998) Methane emission by termites and oxidation by soils, across a forest disturbance gradient in the Mbalmayo Forest Reserve, Cameroon. Glob Chang Biol 4:409–418CrossRefGoogle Scholar
  95. MacDonald JA, Jeeva D, Eggleton P, Davies R, Bignell DE, Fowler D, Lawton J, Maryati M (1999) The effect of termite biomass and anthropogenic disturbance on the CH4 budgets of tropical forests in Cameroon and Borneo. Glob Chang Biol 5:869–879CrossRefGoogle Scholar
  96. Messer AC, Lee MJ (1989) Effect of chemical treatments on methane emission by the hindgut microbiota in the termite Zootermopsis angusticollis. Microb Ecol 18:275–284PubMedPubMedCentralCrossRefGoogle Scholar
  97. Miyata R, Noda N, Tamaki H, Kinjyo K, Aoyagi H, Uchiyama H, Tanaka H (2007) Phylogenetic relationship of symbiotic archaea in the gut of the higher termite Nasutitermes takasagoensis fed with various carbon sources. Microb Environ 22:157–164CrossRefGoogle Scholar
  98. Nardi JB, Bee CM, Taylor SJ (2016) Compartmentalization of microbial communities that inhabit the hindguts of millipedes. Arthropod Struct Dev 45:462–474PubMedPubMedCentralCrossRefGoogle Scholar
  99. Nobu MK, Narihiro T, Kuroda K, Mei R, Liu WT (2016) Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen. ISME J 10:2478–2487PubMedPubMedCentralCrossRefGoogle Scholar
  100. Odelson DA, Breznak JA (1983) Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol 45:1602–1613PubMedPubMedCentralGoogle Scholar
  101. Odelson DA, Breznak JA (1985) Nutrition and growth characteristics of Trichomitopsis termopsidis, a cellulolytic protozoan from termites. Appl Environ Microbiol 49:614–621PubMedPubMedCentralGoogle Scholar
  102. Ohkuma M, Brune A (2011) Diversity, structure, and evolution of the termite gut microbial community. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 413–438Google Scholar
  103. Ohkuma M, Kudo T (1998) Phylogenetic analysis of the symbiotic intestinal microflora of the termite Cryptotermes domesticus. FEMS Microbiol Lett 164:389–395CrossRefGoogle Scholar
  104. Ohkuma M, Noda S, Horikoshi K, Kudo T (1995) Phylogeny of symbiotic methanogens in the gut of the termite Reticulitermes speratus. FEMS Microbiol Lett 134:45–50PubMedPubMedCentralCrossRefGoogle Scholar
  105. Ohkuma M, Noda S, Kudo T (1999) Phylogenetic relationships of symbiotic methanogens in diverse termites. FEMS Microbiol Lett 171:147–153PubMedPubMedCentralCrossRefGoogle Scholar
  106. Paul K, Nonoh JO, Mikulski L, Brune A (2012) “Methanoplasmatales,” Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microbiol 78:8245–8253PubMedPubMedCentralCrossRefGoogle Scholar
  107. Pester M, Brune A (2007) Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J 1:551–565PubMedPubMedCentralCrossRefGoogle Scholar
  108. Pester M, Tholen A, Friedrich MW, Brune A (2007) Methane oxidation in termite hindguts: absence of evidence and evidence of absence. Appl Environ Microbiol 73:2024–2028PubMedPubMedCentralCrossRefGoogle Scholar
  109. Poehlein A, Seedorf H (2016) Draft genome sequences of Methanobrevibacter curvatus DSM11111, Methanobrevibacter cuticularis DSM11139, Methanobrevibacter filiformis DSM11501, and Methanobrevibacter oralis DSM7256. Genome Announc 4:e00617-16PubMedPubMedCentralGoogle Scholar
  110. Purdy KJ (2007) The distribution and diversity of euryarchaeota in termite guts. Adv Appl Microbiol 62:63–80PubMedPubMedCentralCrossRefGoogle Scholar
  111. Radek R (1994) Monocercomonides termitis n. sp., an oxymonad from the lower termite Kalotermes sinaicus. Arch Protistenkunde 144:373–382CrossRefGoogle Scholar
  112. Radek R (1997) Spirotrichonympha minor n. sp., a new hypermastigote termite flagellate. Eur J Protistol 33:361–374CrossRefGoogle Scholar
  113. Rahman NA, Parks DH, Willner DL, Engelbrektson AL, Goffredi SK, Warnecke F, Scheffrahn RH, Hugenholtz P (2015) A molecular survey of Australian and north American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes. Microbiome 3:5PubMedPubMedCentralCrossRefGoogle Scholar
  114. Rasmussen RA, Khalil MAK (1983) Global production of methane by termites. Nature 301:700–702CrossRefGoogle Scholar
  115. Rouland C, Brauman A, Labat M, Lepage M (1993) Nutritional factors affecting methane emission from termites. Chemosphere 26:617–622CrossRefGoogle Scholar
  116. Sanderson MG (1996) Biomass of termites and their emissions of methane and carbon dioxide: a global database. Global Biogeochem Cycles 10:543–557CrossRefGoogle Scholar
  117. Santana RH, Catão ECP, Lopes FAC, Constantino R, Barreto CC, Krüger RH (2015) The gut microbiota of workers of the litter-feeding termite Syntermes wheeleri (Termitidae: Syntermitinae): Archaeal, bacterial, and fungal communities. Microb Ecol 70:545–556PubMedPubMedCentralCrossRefGoogle Scholar
  118. Sawadogo JB, Traoré AS, Dianou D (2012) Seasonal CO2 and CH4 emissions from termite mounds in the sub-Sahelian area of Burkina Faso. Bot Res Int 5:49–56Google Scholar
  119. Schauer C, Thompson CL, Brune A (2012) The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Appl Environ Microbiol 78:2758–2767PubMedPubMedCentralCrossRefGoogle Scholar
  120. Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280PubMedPubMedCentralGoogle Scholar
  121. 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 65:4490–4496PubMedPubMedCentralGoogle Scholar
  122. Schulz K, Hunger S, Brown GG, Tsai SM, Cerri CC, Conrad R, Drake HL (2015) Methanogenic food web in the gut contents of methane-emitting earthworm Eudrilus eugeniae from Brazil. ISME J 9:1778–1792PubMedPubMedCentralCrossRefGoogle Scholar
  123. Seedorf H, Dreisbach A, Hedderich R, Shima S, Thauer RK (2004) F420H2 oxidase (FprA) from Methanobrevibacter arboriphilus, a coenzyme F420-dependent enzyme involved in O2 detoxification. Arch Microbiol 182:126–137PubMedPubMedCentralCrossRefGoogle Scholar
  124. Seiler W, Conrad R, Scharffe D (1984) Field studies of methane emission from termite nests into the atmosphere and measurements of methane uptake by tropical soils. J Atmosph Chem 1:171–186CrossRefGoogle Scholar
  125. Shi Y, Huang Z, Han S, Fan S, Yang H (2015) Phylogenetic diversity of archaea in the intestinal tract of termites from different lineages. J Basic Microbiol 54:1–8Google Scholar
  126. Shinzato N, Yoshino H, Yara K (1992) Methane production by microbial symbionts in the lower and higher termites of the Ryukyu archipelago. In: Sato S, Ishida M, Ishikawa H (eds) Endocytobiology V. Tübingen University Press, Tübingen, pp 161–166Google Scholar
  127. 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 65:837–840PubMedPubMedCentralGoogle Scholar
  128. Shinzato N, Matsumoto T, Yamaoka I, Oshima T, Yamagishi A (2001) Methanogenic symbionts and the locality of their host lower termites. Microb Environ 16:43–47CrossRefGoogle Scholar
  129. Söllinger A, Schwab C, Weinmaier T, Loy A, Tveit AT, Schleper C, Urich T (2016) Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences. FEMS Microbiol Ecol 92:fiv149PubMedPubMedCentralCrossRefGoogle Scholar
  130. Sprenger WW, van Belzen MC, Rosenberg J, Hackstein JHP, Keltjens JT (2000) Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. Int J Syst Evol Microbiol 50:1989–1999PubMedPubMedCentralCrossRefGoogle Scholar
  131. Sprenger WW, Hackstein JHP, Keltjens JT (2005) The energy metabolism of Methanomicrococcus blatticola: physiological and biochemical aspects. Antonie v Leeuwenhoek 87:289–299CrossRefGoogle Scholar
  132. Sprenger WW, Hackstein JH, Keltjens JT (2007) The competitive success of Methanomicrococcus blatticola, a dominant methylotrophic methanogen in the cockroach hindgut, is supported by high substrate affinities and favorable thermodynamics. FEMS Microbiol Ecol 60:266–275PubMedPubMedCentralCrossRefGoogle Scholar
  133. Stubblefield RD, Bennett GA, Shotwell OL, Hall HH, Jackson RD (1966) Organic acids in the haemolymph of healthy and diseased Popillia japonica (Newman) larvae. J Insect Physiol 12:949–956CrossRefGoogle Scholar
  134. Sugimoto A, Inoue T, Kirtibutr N, Abe T (1998a) Methane oxidation by termite mounds estimated by the carbon isotopic composition of methane. Global Biogeochem Cycles 12:595–605CrossRefGoogle Scholar
  135. Sugimoto A, Inoue T, Tayasu I, Miller L, Takeichi S, Abe T (1998b) Methane and hydrogen production in a termite-symbiont system. Ecol Res 13:241–257CrossRefGoogle Scholar
  136. 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 409–435CrossRefGoogle Scholar
  137. Sustr V, Simek M (2009) Methane release from millipedes and other soil invertebrates in Central Europe. Soil Biol Biochem 41:1684–1688CrossRefGoogle Scholar
  138. Sustr V, Chronáková A, Semanová S, Tajovský K, Simek M (2014) Methane production and methanogenic archaea in the digestive tracts of millipedes (Diplopoda). PLoS One 9:e102659PubMedPubMedCentralCrossRefGoogle Scholar
  139. Tang KW, Glud RN, Glud A, Rysgaard S, Nielsen TG (2011) Copepod guts as biogeochemical hotspots in the sea: evidence from microelectrode profiling of Calanus spp. Limnol Oceanogr 56:666–672CrossRefGoogle Scholar
  140. Thauer RK, Kaster A-K, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591PubMedPubMedCentralCrossRefGoogle Scholar
  141. 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 65:4497–4505PubMedPubMedCentralGoogle Scholar
  142. 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 2:436–449PubMedPubMedCentralCrossRefGoogle Scholar
  143. 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
  144. Tholen A, Pester M, Brune A (2007) Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiol Ecol 62:303–312PubMedPubMedCentralCrossRefGoogle Scholar
  145. Tinker KA, Ottesen EA (2016) The core gut microbiome of the American cockroach, Periplaneta americana, is stable and resilient to dietary shifts. Appl Environ Microbiol 82:6603–6610PubMedPubMedCentralCrossRefGoogle Scholar
  146. 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 33:233–240PubMedPubMedCentralCrossRefGoogle Scholar
  147. van Hoek AHAM, van Alen TA, Sprakel VSI, Leunissen JAM, Brigge T, Vogels GD, Hackstein JHP (2000) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 17:251–258PubMedPubMedCentralCrossRefGoogle Scholar
  148. Vogels GD, Hoppe WF, Stumm CK (1980) Association of methanogenic bacteria with rumen ciliates. Appl Environ Microbiol 40:608–612PubMedPubMedCentralGoogle Scholar
  149. Wandiga SO, Mugedo JAZ (1987) Methane emissions by tropical termites feeding on soil, wood, grass, and fungus combs. Kenya J Sci 8A:19–25Google Scholar
  150. Wheeler GS, Tokoro M, Scheffrahn RH, Su N-Y (1996) Comparative respiration and methane production rates in nearctic termites. J Insect Physiol 42:799–806CrossRefGoogle Scholar
  151. Yanase Y, Miura M, Fujii Y, Okumura S, Yoshimura T (2013) Evaluation of the concentrations of hydrogen and methane emitted by termite using a semiconductor gas sensor. J Wood Sci 59:243–248CrossRefGoogle Scholar
  152. Zimmerman PR, Greenberg JP, Wandiga SO, Crutzen PJ (1982) Termites: a potentially large source of atmospheric methane, carbon dioxide, and molecular hydrogen. Science 218:563–565PubMedPubMedCentralCrossRefGoogle Scholar
  153. Zurek L, Keddie BA (1998) Significance of methanogenic symbionts for development of the American cockroach, Periplaneta americana. J Insect Physiol 44:645–651PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Research Group Insect Gut Microbiology and SymbiosisMax Planck Institute for Terrestrial MicrobiologyMarburgGermany

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