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Termite Gut Spirochetes

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The Prokaryotes

Introduction

There are few habitats on earth in which spirochetes are such prominent members of the microbial community as in the hindgut of termites. This was first documented over a century ago by Joseph Leidy (Leidy, 1874–1881; Leidy, 1877), who was struck by their abundance in hindgut contents of the eastern subterranean termite, Termes (now Reticulitermes) flavipes. In some termites, spirochetes account for up to 50% of all prokaryotes in the hindgut (Paster et al., 1996), and even casual phase contrast microscopic observation of hindgut contents usually reveals about a dozen different morphological types, distinguishable on the bases of cell size, wavelength and amplitude, or pitch (Fig. 1).

Fig. 1.
figure 1

A wood-eating termite, Reticulitermes flavipes(top), is positioned next to a gut extracted from a separate individual (middle). Vertical white arrowhead indicates the juncture between the hindgut (left) and tubular midgut (right). Bottom is a phase contrast micrograph of diluted gut...

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Literature Cited

  • Ball, G. H. 1969 Organisms living on and in protozoa In: T.-T. Chen (Ed.) Research in Protozoology Pergamon Press New York NY 565–718

    Google Scholar 

  • Beckwith, T. D., and S. F. Light. 1927 The spirals within the termite gut for class use Science 66 656–657

    Article  PubMed  CAS  Google Scholar 

  • Berchtold, M., W. Ludwig, and H. König. 1994 16S rDNA sequence and phylogenetic position of an uncultivated spirochete from the hindgut of the termite Mastotermes darwiniensis Froggatt FEMS Microbiol. Lett. 123 269–273

    Article  PubMed  CAS  Google Scholar 

  • Berchtold, M., and H. König. 1996 Phylogenetic analysis and in situ identification of uncultivated spirochetes from the hindgut of the termite Mastotermes darwiniensis Syst. Appl. Microbiol. 19 66–73

    Article  Google Scholar 

  • Bermudes, D., D. Chase, and L. Margulis. 1988 Morphology as a basis for taxonomy of large spirochetes symbiotic in wood-eating cockroaches and termites: Pillotina gen. nov., nom. rev.; Pillotina calotermitidis sp. nov., nom. rev.; Diplocalyx gen. nov., nom. rev.; Diplocalyx calotermitidis sp. nov., nom. rev.; Hollandinagen. nov., nom. rev.; Hollandina pterotermitidis sp. nov., nom. rev.; and Clevelandina reticulitermitidis gen. nov., sp. nov Int. J. Syst. Bacteriol. 38 291–302

    Article  PubMed  CAS  Google Scholar 

  • Bignell, D. E., H. Oskarsson, J. M. Anderson, and P. Ineson. 1983 Structure, microbial associations and function of the so-called “mixed segment” of the gut in two soil-feeding termites, Procubitermes aburiensis and Cubitermes severus (Termitidae, Termitinae) J. Zool. Lond. 201 445–480

    Article  Google Scholar 

  • Bloodgood, R. A., K. R. Miller, T. P. Fitzharris, J. R. McIntosh. 1974 The ultrastructure of Pyrsonympha and its associated microorganisms J. Morphol. 143 77–106

    Article  Google Scholar 

  • Bloodgood, R. A., and T. P. Fitzharris. 1976 Specific associations of prokaryotes with symbiotic flagellate protozoa from the hindgut of the termite Reticulitermes and the wood-eating roack Cryptocercus Cytobios 17 103–122

    PubMed  CAS  Google Scholar 

  • Breznak, J. A. 1973 Biology of nonpathogenic, host-associated spirochetes CRC Crit. Rev. Microbiol. 2 457–489

    Article  Google Scholar 

  • Breznak, J. A. 1984 Hindgut spirochetes of termites and Cryptocercus punctulatus In: N. R. Krieg and J. G. Holt (Eds.) Bergey’s Manual of Systematic Bacteriology Williams and Wilkins Baltimore MD 67–70

    Google Scholar 

  • Breznak, J. A., and J. M. Switzer. 1986 Acetate synthesis from H2 plus CO2 by termite gut microbes Appl. Environ. Microbiol. 52 623–630

    PubMed  CAS  Google Scholar 

  • Breznak, J. A. 1994 Acetogenesis from carbon dioxide in termite guts In: H. L. Drake (Ed.) Acetogenesis Chapman and Hall New York NY 303–330

    Chapter  Google Scholar 

  • Breznak, J. A. 2000 Ecology of prokaryotic microbes in the guts of wood-and litter-feeding termites In: T. Abe, D. E. Bignell, and M. Higashi (Eds.) Termites: Evolution, Sociality, Symbiosis, Ecology Kluwer Academic Publishers Dordrecht The Netherlands 209–231

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cleveland, L. R., S. R. Hall, E. P. Sanders, and J. Collier. 1934 The wood-feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach Memoirs Am. Acad. Arts Sci. 17 187–342

    Google Scholar 

  • Cleveland, L. R., and A. V. Grimstone. 1964 The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms Proc. R. Soc. London (Series B) 159 668–686

    Article  Google Scholar 

  • Drake, H. L. 1994 Acetogenesis, acetogenic bacteria, and the acetyl-CoA “Wood/Ljungdahl” pathway: Past and current perspectives In: H. L. Drake (Ed.) Acetogenesis Chapman and Hall New York NY 3–60

    Chapter  Google Scholar 

  • Ebert, A., and A. Brune. 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

    PubMed  CAS  Google Scholar 

  • Eutick, M. L., P. Veivers, R. W. O’Brien, and M. Slaytor. 1978 Dependence of the higher termite, Nasutitermes exitiosus and the lower termite, Coptotermes lacteus on their gut flora J. Insect Physiol. 24 363–368

    Article  CAS  Google Scholar 

  • French, J. R. J., G. L. Turner, and J. F. Bradbury. 1976 Nitrogen fixation by bacteria from the hindgut of termites J. Gen. Microbiol. 95 202–206

    Article  CAS  Google Scholar 

  • Ghidini, G. M., and I. Archetti. 1939 Studi sulle termiti. 2: Le spirochete presenti in Reticulitermes lucifugus Rossi Rivista di Biologia Coloniale 2 125–140

    Google Scholar 

  • Graber, J., and J. A. Breznak. 2000 Abstr. Am. Soc. Microbiol.

    Google Scholar 

  • Grimstone, A. V. 1963 A note on the fine structure of a spirochaete Quart. J. Microsc. Sci. 104 145–153

    Google Scholar 

  • Hollande, A. C., and I. Gharagozlou. 1967 Morphologie infrastructurale de Pillotina calotermitidis nov. gen., nov. sp., spirochaetale de l’intestin de Calotermes praecox C.R. Acad. Sci. (Paris) 265 1309–1312

    CAS  Google Scholar 

  • Hungate, R. E. 1969 A roll tube method for cultivation of strict anaerobes In: J. R. Norris and D. W. Ribbons (Eds.) Methods in Microbiology Academic Press New York NY 117–132

    Google Scholar 

  • Iida, T., M. Ohkuma, K. Ohtoko, and T. Kudo. 2000 Symbiotic spirochetes in the termite hindgut: Phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists FEMS Microbiol. Ecol. 34 17–26

    Article  PubMed  CAS  Google Scholar 

  • Kirby, H. J. 1941 Organisms living on and in protozoa In: G. N. Calkins and F. M. Summers (Eds.) Protozoa in Biological Research Columbia University Press New York NY 1009–1113

    Google Scholar 

  • Kuhnigk, T., J. Branke, D. Krekeler, H. Cypionka, H. Konig. 1996 A feasible role of sulfate-reducing bacteria in the termite gut Syst. Appl. Microbiol. 19 139–149

    Article  CAS  Google Scholar 

  • Leadbetter, J. R., and J. A. Breznak. 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, J. R., T. M. Schmidt, J. R. Graber, and J. A. Breznak. 1999 Acetogenesis from H2 plus CO2 by spirochetes from termite guts Science 283 686–689

    Article  PubMed  CAS  Google Scholar 

  • Leidy, J. 1874–1881 The parasites of the termites J. Acad. Nat. Sci. (Phila.) 8 425–447

    Google Scholar 

  • Leidy, J. 1877 On the intestinal parasites of Termes flavipes Proc. Acad. Nat. Sci. (Phila.) 29 146–149

    Google Scholar 

  • Lilburn, T. G., T. M. Schmidt, and J. A. Breznak. 1999 Phylogenetic diversity of termite gut spirochaetes Environ. Microbiol. 1 331–345

    Article  PubMed  CAS  Google Scholar 

  • Lilburn, T. G., K. S. Kim, N. E. Ostrom, K. R. Byzek, J. R. Leadbetter, and J. A. Breznak. 2001 Nitrogen fixation by symbiotic and free-living spirochetes Science 292 2495–2498

    Article  PubMed  CAS  Google Scholar 

  • Margulis, L., and G. Hinkle. 1992 Large symbiotic spirochetes: Clevelandina, Cristispira, Diplocalyx, Hollandina, and Pillotina In: A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (Eds.) The Prokaryotes, 2nd ed. Springer-Verlag New York NY 3965–3978

    Google Scholar 

  • Miller, J. N., R. M. Smibert, and J. R. Norris. 1992 The genus Treponema In: A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (Eds.) The Prokaryotes, 2nd ed Springer-Verlag New York NY 3537–3559

    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  Google Scholar 

  • Nalepa, C. A., and C. Bandi. 2000 Characterizing the ancestors: Paedomorphosis and termite evolution In: T. Abe, D. E. Bignell, and M. Higashi (Eds.) Termites: Evolution, Sociality, Symbioses, Ecology Kluwer Academic Dordrecht The Netherlands 53–75

    Google Scholar 

  • Noda, S., M. Ohkuma, R. Usami, K. Horikoshi, and T. Kudo. 1999 Culture-independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis Appl. Environ. Microbiol. 65 4935–4942

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ohkuma, M., S. Noda, R. Usami, K. Horikoshi, and T. Kudo. 1996b Diversity of nitrogen fixation genes in the symbiotic intestinal microflora of the termite Reticulitermes speratus Appl. Environ. Microbiol. 62 2747–2752

    PubMed  CAS  Google Scholar 

  • Ohkuma, M., and T. Kudo. 1998 Phylogenetic analysis of the symbiotic intestinal microflora of the termite Cryptotermes domesticus FEMS Microbiol. Lett. 164 389–395

    Article  CAS  Google Scholar 

  • Ohkuma, M., T. Iida, and T. Kudo. 1999a Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites FEMS Microbiol. Lett. 181 123–129

    Article  PubMed  CAS  Google Scholar 

  • Ohkuma, M., S. Noda, and T. Kudo. 1999b Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites Appl. Environ. Microbiol. 65 4926–4934

    PubMed  CAS  Google Scholar 

  • Oremland, R. S. 1988 Biogeochemistry of methanogenic bacteria In: A. J. B. Zehnder (Ed.) Biology of Anaerobic Microorganisms John Wiley New York NY 641–705

    Google Scholar 

  • Paster, B. J. et al. 1991 Phylogenetic analysis of the spirochetes J. Bacteriol. 173 6101–6109

    PubMed  CAS  Google Scholar 

  • Paster, B. J., F. E. Dewhirst, S. M. Cooke, V. Fussing, L. K. Poulsen, and J. A. Breznak. 1996 Phylogeny of not-yet-cultured spirochetes from termite guts Appl. Environ. Microbiol. 62 347–352

    PubMed  CAS  Google Scholar 

  • Potrikus, C. J., and J. A. Breznak. 1977 Nitrogen-fixing Enterobacter agglomerans isolated from guts of wood-eating termites Appl. Environ. Microbiol. 33 392–399

    PubMed  CAS  Google Scholar 

  • Radek, R., K. Hausmann, and A. Breunig. 1992 Ectobiotic and endocytobiotic bacteria associated with the termite flagellate Joenia annectens Acta Protozool. 31 93–107

    Google Scholar 

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

    Article  Google Scholar 

  • Rösel, J., R. Radek, and K. Hausmann. 1996 Ultrastructure of the trichomonad flagellate Stephanonympha nelumbium J. Euk. Microbiol. 43 505–511

    Article  Google Scholar 

  • Smith, H. E., and H. J. Arnott. 1974 Epi-and endobiotic bacteria associated with Pyrsonympha vertens, a symbiotic protozoan of the termite Reticulitermes flavipes Trans. Am. Microsci. Soc. 93 180–194

    Article  CAS  Google Scholar 

  • Smith, H. E., H. E. Buhse Jr., and S. J. Stamler. 1975a Possible formation and development of spirochaete attachment sites found on the surface of symbiotic polymastigote flagellates of the termite Reticulitermes flavipes Biosystems 7 374–379

    Article  PubMed  CAS  Google Scholar 

  • Smith, H. E., S. J. Stamler, and H. E. Buhse. 1975b A scanning electron microscope survey of the surface features of polymastigote flagellates from Reticulitermes flavipes Trans. Am. Microsci. Soc. 94 401–410

    Article  Google Scholar 

  • Stanton, T. B., and E. Canale-Parola. 1979 Enumeration and selective isolation of rumen spirochetes Appl. Environ. Microbiol. 38 965–973

    PubMed  CAS  Google Scholar 

  • Tayasu, I., A. Sugimoto, E. Wada, and T. Abe. 1994 Xylophagous termites depending on atmospheric nitrogen Naturwissenschaften 81 229–231

    Google Scholar 

  • Tholen, A., and A. Brune. 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  PubMed  CAS  Google Scholar 

  • Tokeshi, M. 1993 Species abundance patterns and comunity structure Adv. Ecol. Res. 24 111–186

    Article  Google Scholar 

  • Widdel, F., and N. Pfennig. 1981 Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. I. Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov., sp. nov Arch. Microbiol. 129 395–400

    Article  PubMed  CAS  Google Scholar 

  • Wier, A., J. Ashen, and L. Margulis. 2000 Canaleparolina darwiniensis, gen. nov., and other pillotinaceous spirochetes from insects Int. Microbiol. 3 213–223

    PubMed  CAS  Google Scholar 

  • Wyss, C. 1992 Growth of Porphyromonas gingivalis, Treponema denticola, T. pectinovorum, T. socranskii, and T. vincentii in a chemically defined medium J. Clin. Microbiol. 30 2225–2229

    PubMed  CAS  Google Scholar 

  • Wyss, C., B. K. Choi, P. Schupbach, B. Guggenheim, and U. B. Göbel. 1996 Treponema maltophilum sp. nov., a small oral spirochete isolated from human periodontal lesions Int. J. Syst. Bacteriol. 46 745–752

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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Breznak, J.A., Leadbetter, J.R. (2006). Termite Gut Spirochetes. In: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, KH., Stackebrandt, E. (eds) The Prokaryotes. Springer, New York, NY. https://doi.org/10.1007/0-387-30747-8_11

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