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Termite Gut Flagellates and Their Methanogenic and Eubacterial Symbionts

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Book cover (Endo)symbiotic Methanogenic Archaea

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

Abstract

Termites harbor an abundance and diversity of symbiotic microbes in their gut, which comprise all the three domains of life, Eucarya, Bacteria, and Archaea. One of the most prominent features of this microbiota is the cellular association of the gut flagellates with eubacteria and/or methanogenic archaea. The eubacterial and methanogenic symbionts are observed both inside and on the surface of the host flagellate cells. Recent technological advances in genomics have enabled researchers to predict the functions of these as-yet-uncultivable prokaryotic symbionts, in addition to their phylogenetic positions and specific localizations based on 16S rRNA analyses. Several complete and draft genome sequences of endo- and ectosymbionts of gut flagellates have shown consistency of their functions in spite of their taxonomic diversity.

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References

  • Abdul Rahman N, Parks DH, Willner DL, Engelberktson 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:e5

    Article  Google Scholar 

  • Andrew BJ (1930) Method and rate of protozoan refaunation in the termite Termopsis angusticollis. Hagen Univ Calif (Berkeley) Publ Zool 33:449–470

    Google Scholar 

  • Berchtold M, Chatzinotas A, Schönhuber W, Brune A, Amann R, Hahn D, König H (1999) Differential enumeration and in situ localization of microorganisms in the hindgut of the lower termite Mastotermes darwiniensis by hybridization with rRNA-targeted probes. Arch Microbiol 172:407–416

    Article  CAS  PubMed  Google Scholar 

  • Boucias DG, Cai Y, Sun Y, Lietze VU, 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 22:1836–1853

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brauman A, Dore J, Eggleton P, Bignell DE, Breznak JA, Kane MD (2001) Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol Ecol 35:27–36

    Article  CAS  PubMed  Google Scholar 

  • Breznak JA (2000) Ecology of prokaryotic microbes in the guts of wood- and litter-feeding termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 209–232

    Chapter  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12:168–180

    Article  CAS  PubMed  Google Scholar 

  • Brune A (2017) Ectosymbiotic Endomicrobia – a transition stage towards intracellular symbionts? Environ Microbiol Rep 9:474–476

    Article  PubMed  Google Scholar 

  • Brune A (2018) Methanogens in the digestive tract of termites. In: Hackstein JHP (ed) Microbiology monographs: (Endo)symbiotic methanogenic archaea. Springer-Nature, Heidelberg

    Google Scholar 

  • 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, New York, pp 413–438

    Google Scholar 

  • Brune A, Stingl U (2006) Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis. Prog Mol Subcell Biol 41:39–60

    Article  CAS  PubMed  Google Scholar 

  • Cleveland LR, Grimstone AV (1964) The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Proc R Soc Lond B 159:668–686

    Article  Google Scholar 

  • Deevong P, Hattori M, Yamada A, Trakulnaleamsai S, Ohkuma M, Noparatnaraporn N, Kudo T (2004) Isolation and detection of methanogens from the gut of higher termites. Microbes Environ 19:221–226

    Article  Google Scholar 

  • Desai MS, Brune A (2012) Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. ISME J 6:1302–1313

    Article  CAS  PubMed  Google Scholar 

  • Desai MS, Strassert JFH, Meuser K, Hertel H, Ikeda-Ohtsubo W, Radek R, Brune A (2010) Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environ Microbiol 12:2120–2132

    CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebert A, Brune A (1997) Hydrogen concentration profiles at the oxic-anoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl Environ Microbiol 63:4039–4046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fenchel T, Finlay BJ (2018) Free-living protozoa with endosymbiotic methanogens. In: Hackstein JHP (ed) Microbiology monographs: (Endo)symbiotic methanogenic archaea. Springer-Nature, Heidelberg

    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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graber JR, Leadbetter JR, Breznak JA (2004) Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Appl Environ Microbiol 70:1315–1320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Microbes Environ 19:120–127

    Article  Google Scholar 

  • Hongoh Y (2010) Diversity and genomes of uncultured microbial symbionts in the termite gut. Biosci Biotechnol Biochem 74:1145–1151

    Article  CAS  PubMed  Google Scholar 

  • Hongoh Y (2011) Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell Mol Life Sci 68:1311–1325

    Article  CAS  PubMed  Google Scholar 

  • Hongoh Y, Ohkuma M, Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44:231–242

    Article  CAS  PubMed  Google Scholar 

  • Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Vongkaluang C, Noparatnaraporn N, Kudo T (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71:6590–6599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hongoh Y, Sato T, Dolan MF, Noda S, Ui S, Kudo T, Ohkuma M (2007a) The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the “Synergistes” group. Appl Environ Microbiol 73:6270–6276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hongoh Y, Sato T, Noda S, Ui S, Kudo T, Ohkuma M (2007b) Candidatus Symbiothrix dinenymphae: bristle-like Bacteroidales ectosymbionts of termite gut protists. Environ Microbiol 9:2631–2635

    Article  CAS  PubMed  Google Scholar 

  • Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M (2008a) Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci USA 105:5555–5560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hongoh Y, Sharma VK, Prakash T, Noda S, Toh H, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M (2008b) Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322:1108–1109

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ikeda-Ohtsubo W, Desai M, Stingl U, Brune A (2007) Phylogenetic diversity of ‘Endomicrobia’ and their specific affiliation with termite gut flagellates. Microbiology 153:3458–3465

    Article  CAS  PubMed  Google Scholar 

  • Ikeda-Ohtsubo W, Faivre N, Brune A (2010) Putatively free-living ‘Endomicrobia’ – ancestors of the intracellular symbionts of termite gut flagellates? Environ Microbiol Rep 2:554–559

    Article  PubMed  Google Scholar 

  • Ikeda-Ohtsubo W, Strassert JF, Kohler T, Mikaelyan A, Gregor I, McHardy AC, Tringe SG, Hugenholtz P, Radek R, Brune A (2016) ‘Candidatus Adiutrix intracellularis’, an endosymbiont of termite gut flagellates, is the first representative of a deep-branching clade of Deltaproteobacteria and a putative homoacetogen. Environ Microbiol 18:2548–2564

    Article  CAS  PubMed  Google Scholar 

  • Inoue J, Saita K, Kudo T, Ui S, Ohkuma M (2007) Hydrogen production by termite gut protists: characterization of iron hydrogenases of parabasalian symbionts of the termite Coptotermes formosanus. Eukaryot Cell 6:1925–1932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Microbes Environ 23:94–97

    Article  PubMed  Google Scholar 

  • Izawa K, Kuwahara H, Kihara K, Yuki M, Lo N, Itoh T, Ohkuma M, Hongoh Y (2016) Comparison of intracellular “Ca. Endomicrobium trichonymphae” genomovars illuminates the requirement and decay of defense systems against foreign DNA. Genome Biol Evol 8:3099–3107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izawa K, Kuwahara H, Sugaya K, Lo N, Ohkuma M, Hongoh Y (2017) Discovery of ectosymbiotic Endomicrobium lineages associated with protists in the gut of stolotermitid termites. Environ Microbiol Rep 9:411–418

    Article  CAS  PubMed  Google Scholar 

  • Jenkins TM, Dean RE, Verkerk R, Forschler BT (2001) Phylogenetic analyses of two mitochondrial genes and one nuclear intron region illuminate European subterranean termite (Isoptera: Rhinotermitidae) gene flow, taxonomy, and introduction dynamics. Mol Phylogenet Evol 20:286–293

    Article  CAS  PubMed  Google Scholar 

  • Kirby H (1930) Trichomonad flagellates from termites. Univ Calif (Berkeley) Publ Zool 33:393–444

    Google Scholar 

  • Kirby H (1944) The structural characteristics and nuclear parasites of some species of Trichonympha in termites. Univ Calif (Berkeley) Publ Zool 49:185–282

    Google Scholar 

  • Kitade O (2004) Comparison of symbiotic flagellate faunae between termites and a wood-feeding cockroach of the genus Cryptocercus. Microbes Environ 19:215–220

    Article  Google Scholar 

  • Kitade O, Matsumoto T (1998) Characteristics of the symbiotic flagellate composition within the termite family Rhinotermitidae (Isoptera). Symbiosis 25:271–278

    Google Scholar 

  • Kitade O, Maeyama T, Matsumoto T (1997) Establishment of symbiotic flagellate fauna of Hodotermopsis japonica (Isoptera: Termopsidae). Sociobiology 30:161–167

    Google Scholar 

  • Kuwahara H, Yuki M, Izawa K, Ohkuma M, Hongoh Y (2017) Genome of ‘Ca. Desulfovibrio trichonymphae’, an H2-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut. ISME J 11:766–776

    Article  CAS  PubMed  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

    CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lee MJ, Schreurs PJ, Messer AC, Zinder SH (1987) Association of methanogenic bacteria with flagellated protozoa from a termite gut. Curr Microbiol 15:337–341

    Article  Google Scholar 

  • Lilburn TG, Kim KS, Ostrom NE, Byzek KR, Leadbetter JR, Breznak JA (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mikaelyan A, Köhler T, Lampert N, Rohland J, Boga H, Meuser K, Brune A (2015) Classifying the bacterial gut microbiota of termites and cockroaches: a curated phylogenetic reference database (DictDb). Syst Appl Microbiol 38:472–482

    Article  CAS  PubMed  Google Scholar 

  • Mikaelyan A, Thompson CL, Meuser K, Zheng H, Rani P, Plarre R, Brune A (2017) High-resolution phylogenetic analysis of Endomicrobia reveals multiple acquisitions of endosymbiotic lineages by termite gut flagellates. Environ Microbiol Rep 9:477–483

    Article  CAS  PubMed  Google Scholar 

  • Müller N, Timmers P, Plugge CM, Stams AJM, Schink B (2018) Syntrophy in methanogenic degradation. In: Hackstein JHP (ed) Microbiology monographs: (Endo)symbiotic methanogenic archaea. Springer-Nature, Heidelberg

    Google Scholar 

  • 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 69:625–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noda S, Iida T, Kitade O, Nakajima H, Kudo T, Ohkuma M (2005) Endosymbiotic Bacteroidales bacteria of the flagellated protist Pseudotrichonympha grassii in the gut of the termite Coptotermes formosanus. Appl Environ Microbiol 71:8811–8817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noda S, Inoue T, Hongoh Y, Kawai M, Nalepa CA, Vongkaluang C, Kudo T, Ohkuma M (2006a) Identification and characterization of ectosymbionts of distinct lineages in Bacteroidales attached to flagellated protists in the gut of termites and a wood-feeding cockroach. Environ Microbiol 8:11–20

    Article  CAS  PubMed  Google Scholar 

  • Noda S, Kawai M, Nakajima H, Kudo T, Ohkuma M (2006b) Identification and in situ detection of two lineages of Bacteroidales ectosymbionts associated with a termite gut protist, Oxymonas sp. Microbes Environ 21:16–22

    Article  Google Scholar 

  • Noda S, Kitade O, Inoue T, Kawai M, Kanuka M, Hiroshima K, Hongoh Y, Constantino R, Uys V, Zhong J-H, Kudo T, Ohkuma M (2007) Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol Ecol 16:1257–1266

    Article  CAS  PubMed  Google Scholar 

  • Noda S, Hongoh Y, Sato T, Ohkuma M (2009) Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites. BMC Evol Biol 9:e158

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ohkuma M, Kudo T (1996) Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl Environ Microbiol 62:461–468

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ohkuma M, Sato T, Noda S, Ui S, Kudo T, Hongoh Y (2007) The candidate phylum ‘Termite Group 1’ of bacteria: phylogenetic diversity, distribution, and endosymbiont members of various gut flagellated protists. FEMS Microbiol Ecol 60:467–476

    Article  CAS  PubMed  Google Scholar 

  • Ohkuma M, Noda S, Hattori S, Iida T, Yuki M, Starns D, Inoue J, Darby AC, Hongoh Y (2015) Acetogenesis from H2 plus CO2 and nitrogen fixation by an endosymbiotic spirochete of a termite-gut cellulolytic protist. Proc Natl Acad Sci USA 112:10224–10230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radek R (1999) Flagellates, bacteria, and fungi associated with termites: diversity and function in nutrition – a review. Ecotropica 5:183–196

    Google Scholar 

  • Radek R, Tischendorf G (1999) Bacterial adhesion to different termite flagellates: ultrastructural and functional evidence for distinct molecular attachment modes. Protoplasma 207:43–53

    Article  CAS  Google Scholar 

  • Radek R, Roesel J, Hausmann K (1996) Light and electron microscopic study of the bacterial adhesion to termite flagellates applying lectin cytochemistry. Protoplasma 193:105–122

    Article  Google Scholar 

  • Ramos AR, Grein F, Oliveira GP, Venceslau SS, Keller KL, Wall JD, Pereira IA (2015) The FlxABCD-HdrABC proteins correspond to a novel NADH dehydrogenase/heterodisulfide reductase widespread in anaerobic bacteria and involved in ethanol metabolism in Desulfovibrio vulgaris Hildenborough. Environ Microbiol 17:2288–2305

    Article  CAS  PubMed  Google Scholar 

  • Sato T, Hongoh Y, Noda S, Hattori S, Ui S, Ohkuma M (2009) Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut. Environ Microbiol 11:1007–1015

    Article  PubMed  Google Scholar 

  • Sato T, Kuwahara H, Fujita K, Noda S, Kihara K, Yamada A, Ohkuma M, Hongoh Y (2014) Intranuclear verrucomicrobial symbionts and evidence of lateral gene transfer to the host protist in the termite gut. ISME J 8:1008–1019

    Article  CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stingl U, Maass A, Radek R, Brune A (2004) Symbionts of the gut flagellate Staurojoenina sp. from Neotermes cubanus represent a novel, termite-associated lineage of Bacteroidales: description of ‘Candidatus Vestibaculum illigatum’. Microbiology 150:2229–2235

    Article  CAS  PubMed  Google Scholar 

  • Stingl U, Radek R, Yang H, Brune A (2005) “Endomicrobia”: cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes. Appl Environ Microbiol 71:1473–1479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strassert JFH, Köhler T, Wienemann THG, Ikeda-Ohtsubo W, Faivre N, Franckenberg S, Plarre R, Radek R, Brune A (2012) ‘Candidatus Ancillula trichonymphae’, a novel lineage of endosymbiotic Actinobacteria in termite gut flagellates of the genus Trichonympha. Environ Microbiol 14:3259–3270

    Article  CAS  PubMed  Google Scholar 

  • Strassert JF, Mikaelyan A, Woyke T, Brune A (2016) Genome analysis of ‘Candidatus Ancillula trichonymphae’, first representative of a deep-branching clade of Bifidobacteriales, strengthens evidence for convergent evolution in flagellate endosymbionts. Environ Microbiol Rep. doi:https://doi.org/10.1111/1758-2229.12451

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sugimoto A, Bignell DE, Macdonald J (2000) Global impact of termites on the carbon cycle. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, pp 409–436

    Chapter  Google Scholar 

  • Tai V, James ER, Nalepa CA, Scheffrahn RH, Perlman SJ, Keeling PJ (2015) The role of host phylogeny varies in shaping microbial diversity in the hindguts of lower termites. Appl Environ Microbiol 81:1059–1070

    Article  PubMed  PubMed Central  Google Scholar 

  • Tai V, Carpenter KJ, Weber PK, Nalepa CA, Perlman SJ, Keeling PJ (2016) Genome evolution and nitrogen fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches. Appl Environ Microbiol 82:4682–4695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamm SL (1980) The ultrastructure of prokaryotic-eukaryotic cell junctions. J Cell Sci 44:335–352

    CAS  PubMed  Google Scholar 

  • Tamm SL (1982) Flagellated ectosymbiotic bacteria propel a eukaryotic cell. J Cell Biol 94:697–709

    Article  CAS  PubMed  Google Scholar 

  • Tholen A, Brune A (2000) Impact of oxygen on metabolic fluxes and in situ rates of reductive acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes. Environ Microbiol 2:436–449

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Tsunoda K, Ohmura W, Yoshimura T, Tokoro M (1993) Methane emission by the termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) I. Effects of termite caste, population size and volume of test containers. Wood Res 79:34–40

    CAS  Google Scholar 

  • Wenzel M, Radek R, Brugerolle G, König H (2003) Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. Eur J Protistol 39:11–23

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Yamin MA (1979) Flagellates of the orders Trichomonadida Kirby, Oxymonadida Grassé, and Hypermastigida Grassi and Foà reported from lower termites (Isoptera families Mastotermitidae, Kalotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae, and Serritermitidae) and from the wood-feeding roach Cryptocercus (Dictyoptera: Cryptocercidae). Sociobiology 4:1–120

    Google Scholar 

  • Yamin MA (1980) Cellulose metabolism by the termite flagellate Trichomitopsis termopsidis. Appl Environ Microbiol 39:859–863

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Yuki M, Kuwahara H, Shintani M, Izawa K, Sato T, Starns D, Hongoh Y, Ohkuma M (2015) Dominant ectosymbiotic bacteria of cellulolytic protists in the termite gut also have the potential to digest lignocellulose. Environ Microbiol 17:4942–4953

    Article  CAS  PubMed  Google Scholar 

  • Zheng H, Dietrich C, Thompson CL, Meuser K, Brune A (2015) Population structure of Endomicrobia in single host cells of termite gut flagellates (Trichonympha spp.). Microbes Environ 30:92–98

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng H, Dietrich C, Radek R, Brune A (2016) Endomicrobium proavitum, the first isolate of Endomicrobia class. nov. (phylum Elusimicrobia) – an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase. Environ Microbiol 18:191–204

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Yuichi Hongoh .

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Hongoh, Y., Ohkuma, M. (2018). Termite Gut Flagellates and Their Methanogenic and Eubacterial Symbionts. In: Hackstein, J. (eds) (Endo)symbiotic Methanogenic Archaea. Microbiology Monographs, vol 19. Springer, Cham. https://doi.org/10.1007/978-3-319-98836-8_5

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