Nitrate reduction, nitrous oxide formation, and anaerobic ammonia oxidation to nitrite in the gut of soil-feeding termites (Cubitermes and Ophiotermes spp.)

Environmental Microbiology

Volumn 14, Issue 4, 2012, Pages 860-871

  Ngugi, David Kamanda ^a,b   Brune, Andreas ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; CARBON; NITRATE; NITRITE; NITROGEN; NITROUS OXIDE;

ANIMAL; ARTICLE; CARBON CYCLE; CHEMISTRY; DIGESTIVE SYSTEM; GASTROINTESTINAL TRACT; INTESTINE; ISOPTERA; METABOLISM; MICROBIOLOGY; NITROGEN CYCLE; SOIL; TROPIC CLIMATE;

AMMONIA; ANIMALS; CARBON; CARBON CYCLE; DIGESTIVE SYSTEM; GASTROINTESTINAL TRACT; INTESTINES; ISOPTERA; NITRATES; NITRITES; NITROGEN; NITROGEN CYCLE; NITROUS OXIDE; SOIL; SOIL MICROBIOLOGY; TROPICAL CLIMATE;

CUBITERMES; ISOPTERA;

EID: 84859423473     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02648.x     Document Type: Article

References (58)

1. Bignell, D.E. (2006) Termites as soil engineers and soil processors. In Intestinal Microorganisms of Termites and Other Invertebrates. König, H., and Varma, A. (eds). Berlin, Germany: Springer, pp. 183-220.
2. Bignell, D.E., Oskarsson, H., and Anderson, J.M. (1980) Distribution and abundance of bacteria in the gut of a soil-feeding termite Procubitermes aburiensis (Termitidae, Termitinae). J Gen Microbiol 117: 393-403.
3. Bremner, J.M. (1965) Inorganic forms of nitrogen. In Methods of Soil Analysis. part 2, Black, C.A. (ed.). Madison, WI, USA: American Society of Agronomy, pp. 1179-1237.
4. Brümmer, C., Papen, H., Wassmann, R., and Brüggemann, N. (2009) Termite mounds as hot spots of nitrous oxide emissions in South-Sudanian savanna of Burkina Faso (West Africa). Geophys Res Lett 36: L09814.
5. Brune, A. (2006) Symbiotic associations between termites and prokaryotes. In The Prokaryotes, 3rd ed., Volume 1: Symbiotic Associations, Biotechnology, Applied Microbiology. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E. (eds). New York, USA: Springer, pp. 439-474.
6. Brune, A. (2010) Methanogenesis in the digestive tracts of insects. In Handbook of Hydrocarbon and Lipid Microbiology. Vol. 8. Timmis, K.N. (ed.). Heidelberg, Germany: Springer, pp. 707-728.
7. Brune, A., and Kühl, M. (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42: 1121-1127.
8. Brune, A., and Ohkuma, M. (2011) Role of the termite gut microbiota in symbiotic digestion. In Biology of Termites: A Modern Synthesis. Bignell, D.E., Roisin, Y., and Lo, N. (eds). Dordrecht, The Netherlands: Springer, pp. 439-475.
9. Cataldo, D.A., Haroon, M., Schrader, L.E., and Youngs, V.L. (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6: 71-80.
10. Clément, J.-C., Shrestha, J., Ehrenfeld, J.G., and Jaffé, P.R. (2005) Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biol Biochem 37: 2323-2328.
11. Conrad, R. (1995) Soil microbial processes involved in production and consumption of atmospheric trace gases. Adv Microb Ecol 14: 207-250.
12. 2O, and NO). Microbiol Rev 60: 609-640.
13. Dalsgaard, T., Thamdrup, B., and Canfield, E.D. (2005) Anaerobic ammonia oxidation (anammox) in the marine environment. Res Microbiol 156: 457-464.
14. Davidson, E.A., Chorover, J., and Dail, D.B. (2003) A mechanism of abiotic immobilization of nitrate in forest ecosystems: the ferrous wheel hypothesis. Glob Change Biol 9: 228-236.
15. Dejean, A., and Ruelle, J.E. (1995) Importance of Cubitermes termitaries as shelter for alien incipient termite societies. Insect Soc 42: 129-136.
16. Donovan, S.E., Eggleton, P., Dubbin, W.E., Batchelder, M., and Dibog, L. (2001) The effect of a soil-feeding termite, Cubitermes fungifaber (Isoptera, Termitidae) on soil properties: termites may be an important source of soil microhabitat heterogeneity in tropical forests. Pedobiologia 45: 1-11.
17. Drake, H.L., and Horn, M.A. (2007) As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annu Rev Microbiol 61: 169-189.
18. Eggleton, P. (2011) An introduction to termites: biology, taxonomy and functional morphology. In Biology of Termites: A Modern Synthesis. Bignell, D.E., Roisin, Y., and Lo, N. (eds). Dordrecht, The Netherlands: Springer, pp. 1-26.
19. Eggleton, P., and Tayasu, I. (2001) Feeding groups, life types, and the global ecology of termites. Ecol Res 16: 941-960.
20. Fujita, A., and Abe, T. (2002) Amino acid concentration and distribution of lysozyme and protease activities in the guts of higher termites. Physiol Entomol 27: 76-78.
21. Gödde, M., and Conrad, R. (1999) Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification and denitrification in two soils. Biol Fertil Soils 30: 33-40.
22. 2O-producing microorganisms. Appl Environ Microbiol 69: 1662-1669.
23. Horn, M.A., Mertel, R., Gehre, M., Kästner, M., and Drake, H.L. (2006) In vivo emission of dinitrogen by earthworms via denitrifying bacteria in the gut. Appl Environ Microbiol 72: 1013-1018.
24. Hulth, S., Aller, R.C., and Gilbert, F. (1999) Coupled anoxic nitrification/manganese reduction in marine sediments. Geochim et Cosmochim Acta 63: 49-66.
25. Hynes, R.K., and Knowles, R. (1981) Effect of acetylene on autotrophic and heterotrophic nitrification. Can J Microbiol 28: 334-340.
26. Inward, D.J.G., Vogler, A.P., and Eggleton, P. (2007) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phylogenet Evol 44: 953-967.
27. Isermann, K. (1994) Agriculture's share in the emission of trace gases affecting the climate and some cause-oriented proposals for sufficiently reducing this share. Environ Pollut 83: 95-111.
28. 14C-labeled cellulose, peptidoglycan, and protein by the soil-feeding termite Cubitermes orthognathus. Biol Fertil Soils 33: 166-174.
29. 3 by soil-feeding termites. Biogeochem 78: 267-283.
30. 14C-labeled humic model compounds by soil-feeding termites. Soil Biol Biochem 32: 1281-1291.
31. Jones, D.T., and Eggleton, P. (2011) Global biogeography of termites: a compilation of sources. In Biology of Termites: A Modern Synthesis. Bignell, D.E., Roisin, Y., and Lo, N. (eds). Dordrecht, The Netherlands: Springer, pp. 477-498.
32. Kappler, A., and Brune, A. (2002) Dynamics of redox potential and changes in redox state of iron and humic acids during gut passage in soil-feeding termites (Cubitermes spp.). Soil Biol Biochem 34: 221-227.
33. 2O) by earthworms. Appl Environ Microbiol 63: 1878-1882.
34. Kaspar, H.F., and Tiedje, J.M. (1981) Dissimilatory reduction of nitrate and nitrite in the bovine rumen: nitrous oxide production and the effect of acetylene. Appl Environ Microbiol 41: 705-709.
35. 15N in ammonium by producing nitrous oxide. Soil Sci Soc Am J 61: 462-465.
36. Lavelle, P., Bignell, D., Lepage, M., Wolters, V., Roger, P., Ineson, P., etal. (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Biol 33: 159-193.
37. Liu, H., and Beckenbach, A.T. (1992) Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Mol Phylogenet Evol 1: 41-52.
38. 2O) by earthworms obtained from garden and forest soils. Appl Environ Microbiol 65: 3599-3604.
39. Mohan, S.B., Schmid, M., Jetten, M., and Cole, J. (2004) Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiol Ecol 49: 433-443.
40. Ndiaye, D., Lensi, R., Lepage, M., and Brauman, A. (2004) The effect of the soil-feeding termite Cubitermes niokoloensis on soil microbial activity in a semi-arid savanna in West Africa. Plant Soil 259: 277-286.
41. 15N-based approach. Biogeochem 103: 355-369.
42. Nielsen, L.P. (1992) Denitrification in sediment determined from nitrogen isotope-pairing. FEMS Microbiol Ecol 86: 357-362.
43. Noirot, C. (2001) The gut of termites (Isoptera). Comparative anatomy, systematics, and phylogeny. II. Higher termites (Termitidae). Ann Soc Entomol Fr 37: 431-471.
44. Schmitt-Wagner, D., and Brune, A. (1999) Hydrogen profiles and localization of methanogenic activities in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.). Appl Environ Microbiol 65: 4490-4496.
45. Schmitt-Wagner, D., Friedrich, M.W., Wagner, B., and Brune, A. (2003) Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp.). Appl Environ Microbiol 69: 6007-6017.
46. Sessions, A.L. (2006) Isotope-ratio detection for gas chromatography. J Sep Sci 29: 1946-1961.
47. Shrestha, J., Rich, J., Jaffe, P., Joan, G., and Ehrenfeld, J. (2009) Oxidation of ammonium to nitrite under iron-reducing conditions in wetland soils: laboratory, field demonstrations, and push-pull rate determination. Soil Sci 174: 156-164.
48. Shuster, W.D., Shipitalo, M.J., Subler, S., Aref, S., and McCoy, E.L. (2003) Earthworm additions affect leachate production and nitrogen losses in typical midwestern agroecosystems. J Environ Qual 32: 2132-2139.
49. Simek, M., and Hopkins, D.W. (1999) Regulation of potential denitrification by soil pH in long-term fertilized arable soils. Biol Fertil Soils 30: 41-47.
50. 15N in nitrite or nitrate by producing nitrous oxide. Soil Sci Soc Am J 58: 1108-1116.
51. Stief, P., Poulsena, M., Nielsen, P.L., Brix, H., and Schramm, A. (2009) Nitrous oxide emission by aquatic macrofauna. PNAS 10: 4296-4300.
52. Sugimoto, A., Bignell, D.E., and MacDonald, J.A. (2000) Global impact of termites on the carbon cycle and atmospheric trace gases. In Termites: Evolution, Sociality, Symbioses, and Ecology. Abe, T., Bignell, D.E., and Higashi, M. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 409-435.
53. Tholen, A., and Brune, A. (1999) Localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.). Appl Environ Microbiol 65: 4497-4505.
54. Tholen, A., and 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.
55. Tiedje, J.M. (1989) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In Biology of Anaerobic Microorganisms. Zehnder, A.J.B. (ed.). New York, USA: John Wiley and Sons, pp. 179-303.
56. 2 and controlling environmental factors for tropical rain forest sites in Western Kenya. J Geophys Res 112: D03308. 15 pp. doi:10.1029/2006JD007388.
57. Wright, P.A. (1995) Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198: 273-281.
58. Yoshinari, T., and Knowles, R. (1976) Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria. Biochem Biophys Res Commun 69: 705-710.