Skip to main content

The Wood-Eating Termite Hindgut: Diverse Cellular Symbioses in a Microoxic to Anoxic Environment

  • Chapter
  • First Online:
Anoxia

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 21))

  • 1943 Accesses

Abstract

The wood-eating termites evolved 140 million years ago in the Early Cretaceous. Symbiotic microbial communities developed in their hindguts that allowed them to survive on a diet of lignocelluloses, and coevolved into an obligate association that was vertically transmitted through the colony. A typical gut’s microbial community consists of several types of anaerobic protists and hundreds of prokaryotes, many of which are specialized to the gut, and include novel chemoautotrophic forms. Gut-inhabiting protists harbor ecto- and endosymbiotic prokaryotes that have been studied as analogs of early cellular evolution. Genomic studies have revealed a great deal more molecular genetic diversity in the community than was previously known, and are producing the first complete genomes of the bacterial endosymbionts. Experimental studies of the community have lagged because many of the organisms have proven difficult to culture.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Beisson J, Sonnebon TM (1965) Cytoplasmic inheritance of organization of cell cortex in Paramecium aurelia. Proc Natl Acad Sci USA 53:275

    Article  PubMed  CAS  Google Scholar 

  • Berlanga M, Paster BJ, Guerrero R (2007) Coevolution of symbiotic spirochete diversity in lower termites. Int Microbiol 10:133–139

    PubMed  CAS  Google Scholar 

  • Berlanga M, Paster BJ, Guerrero R (2009) The taxophysiological paradox: changes in the intestinal microbiota of the xylophagous cockroach Cryptocercus punctulatus depending on the physiological state of the host. Int Microbiol 12:227–236

    PubMed  CAS  Google Scholar 

  • Bermudes D, Chase D, Margulis L (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., Dilpoclayx gen. nov., nom. rev., Diploclayx calotermitidis sp. nov., nom. rev., Hollandina gen. 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 

  • Breznak JA (1975) Symbiotic relationships between termites and their intestinal microbiota. In: Symbiosis. Symposia of the society for experimental biology No. 29. Cambridge University Press, Cambridge, pp 559–580

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Brugerolle G, Patterson D (2001) Ultrastructure of Joenia pulchella Grassi, 1917 (Protista, Parabasalia), a reassessment of evolutionary trends in the parabasalids, and a new order Cristamonadida. Org Div Evol 1:147–160

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Brune A, Emerson D, Breznak JA (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 

  • Cepicka I, Hampl V, Kulda J (2010) Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist 161:400–433

    Article  PubMed  Google Scholar 

  • Cleveland LR (1947) Sex produced in the protozoa of Cryptocercus by molting. Science 105:16–18

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Dolan MF (2001) Speciation of termite gut protists: the role of bacterial symbionts. Int Microbiol 4:203–208

    Google Scholar 

  • Dolan MF, Melnitsky H (2005) Patterns of protist-bacteria associations in the gut of the wood-feeding cockroack Cryptocercus. J N C Acad Sci 121:56–60

    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 Env Microbiol 63:4039–4046

    Google Scholar 

  • Engel MS, Grimaldi DA, Krishna K (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Mus Novit 3650:1–27

    Article  Google Scholar 

  • Gharagozlou ID (1968) Aspect infrastructural de Diplocalyx calotermitidis nov. gen nov. sp., spirochaetale de l’intestin de Calotermes flavicollis. C R Acad Sci (Paris) 266:494–496

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

  • Harper JT, Gile GH, James ER, Carpenter KJ, Keeling PJ (2009) The inadequacy of morphology for species and genus delineation in microbial eukaryotes: an example from the parabasalian termite symbiont Coronympha. PLoS One 4:e6577

    Article  PubMed  Google Scholar 

  • Hollande AC, Gharagozlou I (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 

  • 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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Hungate RE (1955) Speculations on the role of symbiosis in evolution. In: Hutner SH, Lwoff A (eds) Biochemistry and physiology of protozoa. Academic, New York, pp 194–195

    Google Scholar 

  • Ikeda-Ohtsubo W, Brune A (2008) Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Mol Ecol 18:332–342

    Article  Google Scholar 

  • Inoue J-I, 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 

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

    Google Scholar 

  • Leidy J (1880) Parasites of the termites. J Acad Nat Sci Phila 8:425–447

    Google Scholar 

  • Lilburn TG, Schmidt TM, Breznak JA (1999) Phylogenetic diversity of termite gut spirochetes. Environ Microbiol 1:331–345

    Article  PubMed  CAS  Google Scholar 

  • Margulis L (1993) Symbiosis in cell evolution, 2nd edn. Freeman, New York

    Google Scholar 

  • Margulis L, Hinkle G (1991) Large symbiotic spirochetes: Clevelandina, Cristispira, Diplocalyx, Hollandina, and Pillotina. In: Balows A, TrĂ¼per HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes, vol IV, 2nd edn. Springer, Berlin, pp 3965–3978

    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  PubMed  CAS  Google Scholar 

  • Strassert JFH, Desai MS, Brune A, Radek R (2009) The true diversity of devescovinid flagellates in the termite Incisitermes marginipennis. Protist 160:522–535

    Article  PubMed  Google Scholar 

  • Strassert JFH, Desai MS, Radek R, Brune A (2010) Identification and localization of the multiple bacterial symbionts of the termite gut flagellate Joenia annectens. Microbiology 156:2068–2079

    Article  PubMed  CAS  Google Scholar 

  • Wier AM, Sacchi L, Dolan MF, Bandi C, MacAllister J, Margulis L (2010) Spirochete attachment ultrastructure: implications for the origin and evolution of cilia. Biol Bull 218:25–35

    PubMed  Google Scholar 

  • Yamin M (1979) Flagellates of the orders Trichomonadida Kirby, Oxymonadida GrassĂ©, and Hypermastigida Grassi & FoĂ  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 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael F. Dolan .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Dolan, M.F. (2012). The Wood-Eating Termite Hindgut: Diverse Cellular Symbioses in a Microoxic to Anoxic Environment. In: Altenbach, A., Bernhard, J., Seckbach, J. (eds) Anoxia. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 21. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1896-8_9

Download citation

Publish with us

Policies and ethics