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Applied and Environmental Microbiology, August 1999, p. 3599-3604, Vol. 65, No. 8
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Evidence for Involvement of Gut-Associated Denitrifying Bacteria in Emission of Nitrous Oxide (N2O) by Earthworms Obtained from Garden and Forest Soils

Carola Matthies,* Anja Grießhammer, Martina Schmittroth, and Harold L. Drake

Department of Ecological Microbiology, BITOEK, University of Bayreuth, 95440 Bayreuth, Germany

Received 1 March 1999/Accepted 23 May 1999

Earthworms (Aporrectodea caliginosa, Lumbricus rubellus, and Octolasion lacteum) obtained from nitrous oxide (N2O)-emitting garden soils emitted 0.14 to 0.87 nmol of N2O h-1 g (fresh weight)-1 under in vivo conditions. L. rubellus obtained from N2O-emitting forest soil also emitted N2O, which confirmed previous observations (G. R. Karsten and H. L. Drake, Appl. Environ. Microbiol. 63:1878-1882, 1997). In contrast, commercially obtained Lumbricus terrestris did not emit N2O; however, such worms emitted N2O when they were fed (i.e., preincubated in) garden soils. A. caliginosa, L. rubellus, and O. lacteum substantially increased the rates of N2O emission of garden soil columns and microcosms. Extrapolation of the data to in situ conditions indicated that N2O emission by earthworms accounted for approximately 33% of the N2O emitted by garden soils. In vivo emission of N2O by earthworms obtained from both garden and forest soils was greatly stimulated when worms were moistened with sterile solutions of nitrate or nitrite; in contrast, ammonium did not stimulate in vivo emission of N2O. In the presence of nitrate, acetylene increased the N2O emission rates of earthworms; in contrast, in the presence of nitrite, acetylene had little or no effect on emission of N2O. In vivo emission of N2O decreased by 80% when earthworms were preincubated in soil supplemented with streptomycin and tetracycline. On a fresh weight basis, the rates of N2O emission of dissected earthworm gut sections were substantially higher than the rates of N2O emission of dissected worms lacking gut sections, indicating that N2O production occurred in the gut rather than on the worm surface. In contrast to living earthworms and gut sections that produced N2O under oxic conditions (i.e., in the presence of air), fresh casts (feces) from N2O-emitting earthworms produced N2O only under anoxic conditions. Collectively, these results indicate that gut-associated denitrifying bacteria are responsible for the in vivo emission of N2O by earthworms and contribute to the N2O that is emitted from certain terrestrial ecosystems.

* Corresponding author. Mailing address: Department of Ecological Microbiology, BITOEK, University of Bayreuth, 95440 Bayreuth, Germany. Phone: (49) (0)921-555 642. Fax: (49) (0)921-555 799. E-mail: carola.matthies{at}bitoek.uni-bayreuth.de.

Applied and Environmental Microbiology, August 1999, p. 3599-3604, Vol. 65, No. 8
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Wust, P. K., Horn, M. A., Henderson, G., Janssen, P. H., Rehm, B. H. A., Drake, H. L. (2009). Gut-Associated Denitrification and In Vivo Emission of Nitrous Oxide by the Earthworm Families Megascolecidae and Lumbricidae in New Zealand. Appl. Environ. Microbiol. 75: 3430-3436 [Abstract] [Full Text]  
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  • Ihssen, J., Horn, M. A., Matthies, C., Gossner, A., Schramm, A., Drake, H. L. (2003). N2O-Producing Microorganisms in the Gut of the Earthworm Aporrectodea caliginosa Are Indicative of Ingested Soil Bacteria. Appl. Environ. Microbiol. 69: 1655-1661 [Abstract] [Full Text]  
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