Skip to main content
SpringerLink
Log in

Diversity, Roles, and Biotechnological Applications of Symbiotic Microorganisms in the Gut of Termite

  • Review Article
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Termites are global pests and can cause serious damage to buildings, crops, and plantation forests. The symbiotic intestinal flora plays an important role in the digestion of cellulose and nitrogen in the life of termites. Termites and their symbiotic microbes in the gut form a synergistic system. These organism work together to digest lignocellulose to make the termites grow on nitrogen deficient food. In this paper, the diversity of symbiotic microorganisms in the gut of termites, including protozoan, spirochetes, actinomycetes, fungus and bacteria, and their role in the digestion of lignocellulose and also the biotechnological applications of these symbiotic microorganisms are discussed. The high efficiency lignocellulose degradation systems of symbiotic microbes in termite gut not only provided a new way of biological energy development, but also has immense prospect in the application of cellulase enzymes. In addition, the study on the symbiotic microorganisms in the gut of termites will also provide a new method for the biological control of termites by the endophytic bacteria in the gut of termites.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT (2007) Metagenomic and fuctional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450(7169):560–565

    Article  CAS  PubMed  Google Scholar 

  2. Eggleton P (2010) An introduction to termites: biology, taxonomy and functional morphology. In: Biology of termites: a modern synthesis. Springer, Dordrecht

    Google Scholar 

  3. Hartke TR, Baer B (2011) The mating biology of termites: a comparative review. Anim Behav 82(5):927–936

    Article  Google Scholar 

  4. 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(13):4691–4701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI (2002) Dual cellulose digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32:777–784

    Article  CAS  PubMed  Google Scholar 

  6. Sun LQ, Hse CY, Shupe T, Sun MJ, Wang XH, Zhao K (2015) Isolation and characterization of an endophytic fungal strain with potent anti-microbial and termicidal activities from Port-Orford-Cedar. J Econ Entomol 108(3):962–968

    Article  CAS  PubMed  Google Scholar 

  7. König H, Fröhlich J, Berchtold M, Wenzel M (2002) Diversity and microhabitats of the hindgut flora of termites. Recent Res Dev Microbiol 6:125–156

    Google Scholar 

  8. König H, Fröhlich J, Hertel H (2006) Diversity and lignocellulolytic activities of cultured microorganisms 6: 271–301

  9. Chouvenc T, Efstathion CA, Elliott ML, Su NY (2013) Extended disease resistance emerging from the faecal nest of a subterranean termite. Proc R Soc B 280(1770):1013–1885

    Article  Google Scholar 

  10. Hongoh Y (2011) Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell Mol Life Sci 68(8):1311–1325

    Article  CAS  PubMed  Google Scholar 

  11. Yamin MA (2010) Axenic cultivation of the cellulolytic flagellate Trichomitopsis termopsidis (Cleveland) from the termite Zootermopsis. J Eukaryot Microbiol 25(4):535–538

    Google Scholar 

  12. Yang H, Peng JX, Liu KY, Hong HZ (2006) Diversity and function of symbiotic microbes in the gut of lower termites. Acta Microbiol Sinica 46(3):496–499

    Google Scholar 

  13. Dröge S, Fröhlich J, Radek R, König H (2006) Spirochaeta coccoides sp. nov., a novel coccoid spirochete from the hindgut of the termite Neotermes castaneus. Appl Environ Microbiol 72(1):392–397

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Dröge S, Fröhlich J, Radek R, König H (2008) Treponema isopterocolens sp. nov., a novel spirochete from the hindgut of the termite Incisitermes tabogae. Int J Syst Evol Microbiol 58:1079–1083

    Article  PubMed  CAS  Google Scholar 

  15. Bi SF, Guo ZK, Jiang N, Jiao RH (2013) New alkaloid from Streptomyces koyangensis residing in Odontotermes formosanus. J Asian Nat Prod Res 15(4):422–425

    Article  CAS  PubMed  Google Scholar 

  16. Harazono K, Yamashita N, Shinzato N, Watanabe Y, Fukatsu T, Kurane R (2003) Isolation and characterization of aromatics-degrading microorganisms from the gut of the lower termite Coptotermes formosanus. Biosci Biotechnol Biochem 67(4):889–892

    Article  CAS  PubMed  Google Scholar 

  17. Gomati V, Ramasamy K, Kumar K, Sivaramaiah N, Mula R (2011) Green house gas emissions from termite ecosystem. Afr J Microbiol Res 5(2):56–64

    Google Scholar 

  18. Wenzel M, Schönig I, Berchtold M, Kämpfer P, König H (2002) Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92(1):32–40

    Article  CAS  PubMed  Google Scholar 

  19. 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(23):8245–8253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Guo C, Sun LQ, Kong D, Sun MJ, Zhao K (2014) Klebsiella variicola, a nitrogen fixing activity endophytic bacterium isolated from the gut of Odontotermes formaosanus. Afr J Microbiol Res 8(12):1322–1330

    Article  CAS  Google Scholar 

  21. Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12(3):168–180

    Article  CAS  PubMed  Google Scholar 

  22. Strassert JF, Köhler T, Wienemann TH, Ikeda-Ohtsubo W, Faivre N (2012) ‘Candidatus Ancillula trichonymphae’, a novel lineage of endosymbiotic Actinobacteria in termite gut flagellates of the genus Trichonympha. Environ Microbiol 14(12):3259–3270

    Article  CAS  PubMed  Google Scholar 

  23. Ohkuma M, Ohtoko K, Iida T, Tokura M, Moriya S, Usami R, Horikoshi K, Kudo T (2000) Phylogenetic identification of hypermastigote, Pseudotrichonympha, Spirotrichonympha, Holomastigotoides, and parabasalian symbionts in the hindgut of termites. J Eukaryot Microbiol 47(3):249–259

    Article  CAS  PubMed  Google Scholar 

  24. 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(2):231–242

    Article  CAS  PubMed  Google Scholar 

  25. Petersona BF, Stewart HL, Scharf ME (2015) Quantification of symbiotic contributions to lower termite lignocellulose digestion using antimicrobial treatments. Insect Biochem Mol Biol 59:80–88

    Article  CAS  Google Scholar 

  26. 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 

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

    Article  CAS  PubMed  Google Scholar 

  28. Berlanga M, Paster BJ, Guerrero R (2007) Co-evolution of symbiotic spirochete diversity in lower termites. Int Microbiol 10(2):133–139

    CAS  PubMed  Google Scholar 

  29. Sujada N, Sungthong R, Lumyong S (2014) Termite nests as an abundant source of cultivable antibacteria for biotechnological purpose. Microbes Environ 29(2):211–219

    Article  PubMed  PubMed Central  Google Scholar 

  30. Lefebvre T, Miambi E, Pando A, Diouf M, Rouland-Lefèvre C (2009) Gut-specific actinobacterial community structure and diversity associated with the wood-feeding termite species, nasutitermes corniger, (motschulsky) described by nested pcr-dgge analysis. Insect Soc 56(3):269–276

    Article  Google Scholar 

  31. Fall S, Hamelin J, Ndiaye F, Assigbetse K, Aragno M, Chotte JL (2007) Differences between bacterial communities in the gut of a soil-feeding termite (Cubitermes niokoloensis) and its mounds. Appl Environ Microbiol 73(16):5199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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. Arch Microbiol 172(6):407–416

    Article  CAS  PubMed  Google Scholar 

  33. Hethener P, Brauman A, Garcia JL (1992) Clostridium termitidis sp. nov., a cellulolytic bacterium from the gut of the wood-feeding termite, Nasutitermes lujae. Syst Appl Microbiol 15(1):52–58

    Article  CAS  Google Scholar 

  34. Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3(3):336–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Shinzato N, Muramatsu M, Matsui T, Watanabe Y (2007) Phylogenetic analysis of the gut bacterial microflora of the fungus-growing termite Odontotermes formosanus. Biosci Biotechnol Biochem 71(4):906–915

    Article  CAS  PubMed  Google Scholar 

  36. Bauer S, Tholen A, Overmann J, Brune A (2000) Characterzation of abundance and diversity of lactic acid bacteria in the hindgut of wood- and soil-feeding termites by molecular and culture-dependent techniques. Arch Microbiol 173(2):126–137

    Article  CAS  PubMed  Google Scholar 

  37. Leadbetter JR, Crosby LD, Breznak JA (1998) Methanobrevibacter Filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch Microbiol 169(4):287–292

    Article  CAS  PubMed  Google Scholar 

  38. Veivers PC, Mühlemann R, Slaytor M, Leuthold RH, Bignell DE (1991) Digestion, diet and polyethism in two fungus-growing termites: Macrotermes subhyalinus Rambur and M. michaelseni Sjøstedt. J Insect Physiol 37(9):675–682

    Article  CAS  Google Scholar 

  39. Zhao K, Liu J, Li ZG, Chang ZW, Shi PF, Ping WX, Zhou DP (2011) Bacillus subtilis subspecies virginiana, a new subspecies of antitermitic compound-producing endophytic bacteria isolated from uniperus virginiana. J Econ Entomol 104(5):1502–1508

    Article  CAS  PubMed  Google Scholar 

  40. Deng T, Zhou Y, Cheng M, Pan C, Chen C, Mo J (2008) Synergistic activities of the symbiotic fungus termitomyces albuminosus on the cellulase of odontotermes formosanus (Isoptera: termitidae). Sociobiology 51(3):733–740

    Google Scholar 

  41. Tokuda G, Watanabe H, Hojo M, Fujita A, Makiya H, Arakawa G, Arioka M (2012) Cellulolytic enviroment in the midgut of the wood-feeding higher termite Nasutitermes takasagoensis. J Insect Physiol 58(1):147–154

    Article  CAS  PubMed  Google Scholar 

  42. Wu T, Kong D, Sun LQ, Guo C, Sun MJ, Zhao K (2014) Identification of a nitrogen fixation endophyte from Odontotermes formosanus. J Pure Appl Microbiol 8(2):1669–1674

    CAS  Google Scholar 

  43. Tokuda G, Lo N, Watanabe H (2005) Marked variations in patterns of cellulase activity against crystalline vs. carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol Entomol 30(4):372–380

    CAS  Google Scholar 

  44. Bakalidou A, Kämpfer P, Berchtold M, Kuhnigk T, Wenzel M, König H (2002) Cellulosimicrobium variabile sp. nov., a cellulolytic bacterium from the hindgut of the termite Mastotermes darwiniensis. Int J Syst Evol Microbiol 52(4):1185–1192

    CAS  PubMed  Google Scholar 

  45. 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(3):1059–1070

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Arakawa G, Watanabe H, Yamasaki H, Maekawa H, Tokuda G (2009) Purification and molecular cloning of xylanases from the wood-feeding termite, C. formosanus Shiraki. Biosci Biotechnol Biochem 73:710–718

    Article  CAS  PubMed  Google Scholar 

  47. Pester M, Brune A (2007) Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. Isme J 1(6):551–565

    Article  CAS  PubMed  Google Scholar 

  48. Konig H, Li L, Fröhlich J (2013) The cellulolytic system of the termite gut. Appl Microbiol Biotechnol 97(18):7943–7962

    Article  PubMed  CAS  Google Scholar 

  49. Cleveland LR (1925) The method by which Trichonympha campanula, a protozoön in the intestine of termites, ingests solid particles of wood for food. Biol Bull 48(4):282–288

    Article  CAS  Google Scholar 

  50. Hungate RE (1941) Experiments on the nitrogen economy of termites. Ann Entomol Soc Am 34(2):467–489

    Article  CAS  Google Scholar 

  51. Benemann JR (1973) Nitrogen fixation in termites. Science 181(4095):164–165

    Article  CAS  PubMed  Google Scholar 

  52. Breznak JA, Brill WJ, MertinsJ W, Coppel HC (1973) Nitrogen fixation in termites. Nature 244(5418):577–580

    Article  CAS  PubMed  Google Scholar 

  53. Yamada A, Inoue T, Wiwatwitaya D, Ohkuma M, Kudo T, Sugimoto A (2006) Nitrogen fixation by termites in tropical forests, Thailand. Ecosystems 9(1):75–83

    Article  CAS  Google Scholar 

  54. Meuti ME, Jones SC, Curtis AS (2010) 5N Discrimination and the sensitivity of nitrogen fixation to changes in dietary nitrogen in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Environ Entomol 39(6):1810–1815

    Article  PubMed  Google Scholar 

  55. Scharf ME, Karl ZJ, Sethi A (2011) Defining host-symbiont collaboration in termite lignocellulose digestion: “The view from the tip of the iceberg”. Commun Integr Biol 4(6):761–763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Castro AM, Pereira N Jr (2010) Production, properties and application of cellulases in the hydrolysis of agroindustrial residues. Quim Nova 33(1):181–188

    Article  Google Scholar 

  57. Sun J, Zhou XJ (2011) Utilization of lignocellulose-feeding insects for viable biofuels: an emerging and promising area of entomological science. In: Recent advances in entomological research. Springer, Berlin Heidelberg, pp 434–500

    Chapter  Google Scholar 

  58. Sun JZ, Chen CR (2010) Cellulolytic insects and their potentials for viable biofuels: a new frontier discipline in entomology and bioengineering. Chin Bull Entomol 47(6):1033–1042

    CAS  Google Scholar 

  59. Singh A, Olsen SI (2011) A critical review of biochemical conversion, sustainability and life cycle assessment of algal biofuels. Appl Energy 88(10):3548–3555

    Article  CAS  Google Scholar 

  60. Liu J, Cao D, Zhao K, Ping WX, Zhou DP (2008) Separating endophytes from Port-Orford-Cedar. J Sci Teachers' Coll Univ 4:62–64

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported in part by the Technological innovation talent of special funds for outstanding subject leaders in Harbin (2014RFXXJ081) and Special Project of Graduate Entrepreneurship of Heilongjiang University (20170160908).

Author information

Authors and Affiliations

  1. Key Laboratory of Microbiology, School of Life Science, Heilongjiang University, Harbin, 150080, China

    Jing Zhou, Jiwei Duan, Ying Wang, Xiaohua Wang & Kai Zhao

  2. Heilongjiang University Library, Heilongjiang University, Harbin, 150080, China

    Xiaohua Wang

  3. College of Animal Science and Technology, Northeast Agriculture University, Harbin, 150030, China

    Mingkun Gao

Authors
  1. Jing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiwei Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mingkun Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaohua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kai Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiaohua Wang or Kai Zhao.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest in this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, J., Duan, J., Gao, M. et al. Diversity, Roles, and Biotechnological Applications of Symbiotic Microorganisms in the Gut of Termite. Curr Microbiol 76, 755–761 (2019). https://doi.org/10.1007/s00284-018-1502-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-018-1502-4

Search

Navigation