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Methanogens in the Gastro-Intestinal Tract of Animals

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(Endo)symbiotic Methanogenic Archaea

Part of the book series: Microbiology Monographs ((MICROMONO,volume 19))

Abstract

Nearly all vertebrates host methanogens in their gastro-intestinal tracts. However, a great fraction of vertebrates emits only traces of methane from their faeces (∼1 nmol/g faeces/h) and has no significant amounts of methane in their breath. In contrast, many animals host some 100 times more methanogens in their gastro-intestinal tract and emit methane in their breath. These substantial differences are not caused by different feeding habits; rather a genetic factor controls the presence of large amounts of methanogens. The attribute “methane production” is evolutionarily stable, and the loss of this character obeys Dollo’s law: once lost in the course of evolution, this character cannot be acquired another time.

Also invertebrates can host methanogens in their gastro-intestinal tract. In contrast to the vertebrates, only a few taxa of arthropods emit methane: millipedes, termites, cockroaches and scarab beetles. All other arthropods in our study did not emit methane and did not host even traces of methanogens. As in vertebrates, the diet of the animals is not crucial for the presence of methanogens. Again, a genetic factor seems to control the presence or absence of methanogens. Methanogenesis is also a prerequisite for the presence of intestinal anaerobic protozoa with endosymbiotic methanogens, but not for the presence of impressive structural differentiations of the hindgut epithelium, which – in methanogenic taxa – host enormous amounts of methanogens.

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References

  • Bayon C (1980) Volatile fatty-acids and methane production in relation to anaerobic carbohydrate fermentation in Oryctes nasicornis larvae (Coleoptera, Scarabaeidae). J Insect Physiol 26:819–828

    Article  CAS  Google Scholar 

  • 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 35:5357–5368

    Article  PubMed  CAS  Google Scholar 

  • 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 35:27–36

    Article  PubMed  CAS  Google Scholar 

  • Brune A (2006) Symbiotic associations between termites and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schliefer K-H, Stackebrandt E (eds) The prokaryotes, vol 1, 3rd edn, Symbiotic associations, biotechnology, applied microbiology. Springer, New York, pp 439–474

    Chapter  Google Scholar 

  • Brune A, Emerson D, Breznak J (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 61:2681–2687

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Brusa T, Canzi E, Allievi L, Delpuppo E, Ferrari A (1993) Methanogens in the human intestinal-tract and oral cavity. Curr Microbiol 27:261–265

    Article  Google Scholar 

  • Buchner P (1953) Endosymbiose der Tiere mit pflanzlichen Mikroorganismen. Verlag Birkhäuser, Basel, Stuttgart (English translation: Endosymbiosis of animals with plant microorganisms, Interscience, New York, 1965)

    Google Scholar 

  • Canback B, Tamas I, Andersson SGE (2004) A phylogenomic study of endosymbiotic bacteria. Mol Biol Evol 21:1110–1122

    Article  PubMed  Google Scholar 

  • Cazemier AE, Hackstein JHP, op den Camp HJM, Rosenberg J, van der Drift C (1997) Bacteria in the intestinal tract of different species of arthropods. Microb Ecol 33:189–197

    Article  PubMed  Google Scholar 

  • Cooper A, Mourer-Chauvire C, Chambers GK, von Haeseler A, Wilson A, Pääbo S (1992) Independent origins of New Zealand Moas and Kiwis. Proc Natl Acad Sci USA 89:8741–8744

    Article  PubMed  CAS  Google Scholar 

  • Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465

    Article  PubMed  CAS  Google Scholar 

  • Dettner K, Peters W (2003) Lehrbuch der Entomologie, 2nd edn. Gustav Fischer, Stuttgart

    Google Scholar 

  • Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92

    Article  PubMed  CAS  Google Scholar 

  • Doddema HJ, Vogels GD (1978) Improved identification of methanogenic bacteria by fluorescence microscopy. Appl Environ Microbiol 36:752–754

    PubMed  CAS  Google Scholar 

  • 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 70:3884–3892

    Article  PubMed  CAS  Google Scholar 

  • Doré J, Pochart P, Bernalier A, Goderel I, Morvan B, Rambaud JC (1995) Enumeration of H2-utilizing methanogenic archaea, acetogenic and sulfate-reducing bacteria from human feces. FEMS Microbiol Ecol 17:279–284

    Article  Google Scholar 

  • 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 69:6659–6668

    Article  PubMed  CAS  Google Scholar 

  • El Oufir L, Flourie B, desVarannes SB, Barry JL, Cloarec D, Bornet F, Galmiche JP (1996) Relations between transit time, fermentation products, and hydrogen consuming flora in healthy humans. Gut 38:870–877

    Article  PubMed  CAS  Google Scholar 

  • Fenchel T, Finlay BJ (1995) Ecology and evolution in anoxic worlds. Oxford University Press, Oxford, New York, Tokyo

    Google Scholar 

  • Fenchel T, Finlay BJ (2010) Free-living protozoa with endosymbiotic methanogens. In: Hackstein JHP (ed) (Endo)symbiotic methanogens. Springer, Heidelberg

    Google Scholar 

  • Florin THJ, Jabbar IA (1994) A possible role for bile-acid in the control of methanogenesis and the accumulation of hydrogen gas in the human colon. J Gastroenterol Hepatol 9:112–117

    Article  PubMed  CAS  Google Scholar 

  • Florin THJ, Zhu G, Kirk KM, Martin NG (2000) Shared and unique environmental factors determine the ecology of methanogens in humans and rats. Am J Gastroenterol 95:2872–2879

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hackstein JHP (1997) Eukaryotic molecular biodiversity: systematic approaches for the assessment of symbiotic associations. Antonie Van Leeuwenhoek 72:63–76

    Article  PubMed  CAS  Google Scholar 

  • Hackstein JHP, Stumm CK (1994) Methane production in terrestrial arthropods. Proc Natl Acad Sci USA 91:5441–5445

    Article  PubMed  CAS  Google Scholar 

  • Hackstein JHP, van Alen TA (1996) Fecal methanogens and vertebrate evolution. Evolution 50:559–572

    Article  Google Scholar 

  • Hackstein JHP, van Alen TA, op den Camp HJM, Smits A, Mariman E (1995) Intestinal methanogenesis in primates – a genetic and evolutionary approach. Dtsch Tierarztl Wochenschr 102:152–154

    PubMed  CAS  Google Scholar 

  • Hackstein JHP, Langer P, Rosenberg J (1996) Genetic and evolutionary constraints for the symbiosis between animals and methanogenic bacteria. Environ Monit Assess 42:39–56

    Article  CAS  Google Scholar 

  • Hackstein JHP, van Hoek AHAM, Leunissen JAM, Huynen M (2002) Anaerobic ciliates and their methanogenic endosymbionts. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic Publishers, Doordrecht, The Netherlands, pp 451–464, ISBN 1-4020-0189-4

    Google Scholar 

  • Hackstein JHP, Tjaden J, Huynen M (2006a) Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering! Curr Genet 50:225–245

    Article  PubMed  CAS  Google Scholar 

  • Hackstein JHP, van Alen TA, Rosenberg J (2006b) Methane production by terrestrial arthropods. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Soil biology, vol 6, Manual for soil analysis. Springer, Heidelberg, pp 155–180

    Chapter  Google Scholar 

  • Hackstein JHP, Tielens AGM (2010) Hydrogenosomes. In: Hackstein JHP (ed) (Endo)symbiotic methanogens. Springer, Heidelberg

    Google Scholar 

  • Hoffmeister M, Martin W (2003) Interspecific evolution: microbial symbiosis, endosymbiosis and gene transfer. Env Microbiol 5:641–649

    Article  CAS  Google Scholar 

  • Hudson MJ, Tomkins AM, Wiggins HS, Drasar BS (1993) Breath methane excretion and intestinal methanogenesis in children and adults in rural Nigeria. Scand J Gastroenterol 28:993–998

    Article  PubMed  CAS  Google Scholar 

  • Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Pääbo S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256

    PubMed  CAS  Google Scholar 

  • Jesse BW, Wang L-Q, Baldwin RI (1994) Genetic regulation of postnatal metabolic development. Proc Soc Nutritional Physiol 3:287–288

    Google Scholar 

  • Lange M, Westerman P, Ahring BK (2005) Archaea in protozoa and metazoa. Appl Microbiol Biotechnol 66:465–474

    Article  PubMed  CAS  Google Scholar 

  • Langer P (1988) The mammalian herbivore stomach. Comparative anatomy, function, and evolution. Gustav Fischer, Stuttgart, New York

    Google Scholar 

  • Langer P (1991) Evolution of the digestive tract in mammals. Verh Dtsch Zool Ges 84:169–193

    Google Scholar 

  • Langer P (1994) Food and digestion of cenozoic mammals in europe. In: Chivers DJ, Langer P (eds) The digestive systems in mammals: food, form, and function. Cambridge University Press, Cambridge, pp 9–24

    Chapter  Google Scholar 

  • Langer P, Snipes RL (1991) Adaptations of gut structure to function in herbivores. In: Tsuda T, Sasaki Y, Kawashima R (eds) Physiological aspects of digestions and metabolism in ruminants. Academic, San Diego, pp 349–384

    Chapter  Google Scholar 

  • Leadbetter JR, Breznak JA (1996) Physiological ecology of Methanobrevibacter cuticularis sp nov and Methanobrevibacter curvatus sp nov, isolated from the hindgut of the termite Reticulitermes flavipes. Appl Environ Microbiol 62:3620–3631

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lemke T, van Alen T, Hackstein JHP, Brune A (2001) Cross-epithelial hydrogen transfer from the midgut compartment drives methanogenesis in the hindgut of cockroaches. Appl Environ Microbiol 67:4657–4661

    Article  PubMed  CAS  Google Scholar 

  • Levitt MD, Furne JK, Kuskowski M, Ruddy J (2006) Stability of human methanogenic flora over 35 years and a review of insights obtained from breath methane measurements. Clin Gastroenterol Hepatol 4:123–129

    Article  PubMed  CAS  Google Scholar 

  • Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008a) Evolution of mammals and their gut microbes. Science 320:1647–1651

    Article  PubMed  CAS  Google Scholar 

  • Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008b) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788

    Article  PubMed  CAS  Google Scholar 

  • Li WH, Gouy M, Sharp PM, Uigin CO, Yang YW (1990) Molecular phylogeny of rodentia, lagomorpha, primates, artiodactyla, and carnivora and molecular clocks. Proc Natl Acad Sci USA 87:6703–6707

    Article  PubMed  CAS  Google Scholar 

  • Liu YC, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. In: Wiegel J, Maier RJ, Adams MWW (eds) Incredible anaerobes: from physiology to genomics to fuels. Ann N Y Acad Sci, vol 1125, pp 171–189

    Google Scholar 

  • Miller TL, Wolin MJ (1982) Enumeration of Methanobrevibacter smithii in human feces. Arch Microbiol 131:14–18

    Article  PubMed  CAS  Google Scholar 

  • Miller TL, Wolin MJ (1986) Methanogens in human and animal intestinal tracts. Syst Appl Microbiol 7:223–229

    Article  CAS  Google Scholar 

  • Miyamoto MM, Goodman M (1986) Biomolecular systematics of eutherian mammals – phylogenetic patterns and classification. Syst Zool 35:230–240

    Article  Google Scholar 

  • Miyata R, Noda N, Tamaki H, Kinjyo K, Aoyagi H, Uchiyamai H, Tanaka H (2007) Phylogenetic relationship of symbiotic archaea in the gut of the higher termite Nasutitermes takasagoensis fed with various carbon sources. Microbes Environ 22:157–164

    Article  Google Scholar 

  • Moran NA (2003) Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6:512–518

    Article  PubMed  CAS  Google Scholar 

  • Moran NA (2007) Symbiosis as an adative process and source of phenotypic complexity. Proc Natl Acad Sci USA 104(suppl 1):8627–8633

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Baumann P (2000) Bacterial endosymbionts in animals. Curr Opin Microbiol 3:270–275

    Article  PubMed  CAS  Google Scholar 

  • Moya A, Pereto J, Gil R, Latorre A (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9:218–229

    Article  PubMed  CAS  Google Scholar 

  • Novacek MJ (1992) Mammalian phylogeny – shaking the tree. Nature 356:121–125

    Article  PubMed  CAS  Google Scholar 

  • Ohkuma M, Noda S, Horikoshi K, Kudo T (1995) Phylogeny of symbiotic methanogens in the gut of the termite Reticulitermes speratus. FEMS Microbiol Lett 134:45–50

    Article  PubMed  CAS  Google Scholar 

  • Ohkuma M, Noda S, Kudo T (1999) Phylogenetic relationships of symbiotic methanogens in diverse termites. FEMS Microbiol Lett 171:147–153

    Article  PubMed  CAS  Google Scholar 

  • Ruby EG (2008) Symbiotic conversations are revealed under genetic interrogation. Nat Rev Microbiol 6:752–762

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Segal I, Walker ARP, Lord S, Cummings JH (1988) Breath methane and large bowel-cancer risk in contrasting African populations. Gut 29:608–613

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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 50:1989–1999

    Article  PubMed  CAS  Google Scholar 

  • Stams AJM, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568–577

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • van Hoek AHAM, van Alen TA, Sprakel VSI, Hackstein JHP, Vogels GD (1998) Evolution of anaerobic ciliates from the gastrointestinal tract: phylogenetic analysis of the ribosomal repeat from Nyctotherus ovalis and its relatives. Mol Biol Evol 15:1195–1206

    Article  PubMed  Google Scholar 

  • 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 17:251–258

    Article  PubMed  Google Scholar 

  • 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 XN, Hernandez 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 450:560–565

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms – proposal for the domains archaea, bacteria, and eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

  • Worm P, Müller N, Plugge CM, Stams AJM, Schink B (2010) Syntrophy in methanogenic degradation. In: Hackstein JHP (ed) (Endo)symbiotic methanogens. Springer, Heidelberg

    Google Scholar 

  • Zoetendal EG, Vaughan EE, de Vos WM (2006) A microbial world within us. Mol Microbiol 59:1639–1650

    Article  PubMed  CAS  Google Scholar 

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Hackstein, J.H.P., van Alen, T.A. (2010). Methanogens in the Gastro-Intestinal Tract of Animals. In: Hackstein, J. (eds) (Endo)symbiotic Methanogenic Archaea. Microbiology Monographs, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13615-3_8

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