This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ihssen, J. Articles by Drake, H. L. Search for Related Content PubMed PubMed Citation Articles by Ihssen, J. Articles by Drake, H. L. Agricola Articles by Ihssen, J. Articles by Drake, H. L.

N₂O-Producing Microorganisms in the Gut of the Earthworm Aporrectodea caliginosa Are Indicative of Ingested Soil Bacteria

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

Received 14 November 2002/ Accepted 26 November 2002

The main objectives of this study were (i) to determine if gut wall-associated microorganisms are responsible for the capacity of earthworms to emit nitrous oxide (N₂O) and (ii) to characterize the N₂O-producing bacteria of the earthworm gut. The production of N₂O in the gut of garden soil earthworms (Aporrectodea caliginosa) was mostly associated with the gut contents rather than the gut wall. Under anoxic conditions, nitrite and N₂O were transient products when supplemental nitrate was reduced to N₂ by gut content homogenates. In contrast, nitrite and N₂O were essentially not produced by nitrate-supplemented soil homogenates. The most probable numbers of fermentative anaerobes and microbes that used nitrate as a terminal electron acceptor were approximately 2 orders of magnitude higher in the earthworm gut than in the soil from which the earthworms originated. The fermentative anaerobes in the gut and soil displayed similar physiological functionalities. A total of 136 N₂O-producing isolates that reduced either nitrate or nitrite were obtained from high serial dilutions of gut homogenates. Of the 25 representative N₂O-producing isolates that were chosen for characterization, 22 isolates exhibited >99% 16S rRNA gene sequence similarity with their closest cultured relatives, which in most cases was a soil bacterium, most isolates were affiliated with the gamma subclass of the class Proteobacteria or with the gram-positive bacteria with low DNA G+C contents, and 5 isolates were denitrifiers and reduced nitrate to N₂O or N₂. The initial N₂O production rates of denitrifiers were 1 to 2 orders of magnitude greater than those of the nondenitrifying isolates. However, most nondenitrifying nitrate dissimilators produced nitrite and might therefore indirectly stimulate the production of N₂O via nitrite-utilizing denitrifiers in the gut. The results of this study suggest that most of the N₂O emitted by earthworms is due to the activation of ingested denitrifiers and other nitrate-dissimilating bacteria in the gut lumen.

This article has been cited by other articles:

• Worthen, P. L., Gode, C. J., Graf, J. (2006). Culture-independent characterization of the digestive-tract microbiota of the medicinal leech reveals a tripartite symbiosis.. Appl. Environ. Microbiol. 72: 4775-4781 [Abstract] [Full Text]  
• Horn, M. A., Mertel, R., Gehre, M., Kastner, M., Drake, H. L. (2006). In Vivo Emission of Dinitrogen by Earthworms via Denitrifying Bacteria in the Gut. Appl. Environ. Microbiol. 72: 1013-1018 [Abstract] [Full Text]  
• Horn, M. A., Drake, H. L., Schramm, A. (2006). Nitrous Oxide Reductase Genes (nosZ) of Denitrifying Microbial Populations in Soil and the Earthworm Gut Are Phylogenetically Similar. Appl. Environ. Microbiol. 72: 1019-1026 [Abstract] [Full Text]  
• Davidson, S. K., Stahl, D. A. (2006). Transmission of Nephridial Bacteria of the Earthworm Eisenia fetida. Appl. Environ. Microbiol. 72: 769-775 [Abstract] [Full Text]  
• Horn, M. A., Ihssen, J., Matthies, C., Schramm, A., Acker, G., Drake, H. L. (2005). Dechloromonas denitrificans sp. nov., Flavobacterium denitrificans sp. nov., Paenibacillus anaericanus sp. nov. and Paenibacillus terrae strain MH72, N2O-producing bacteria isolated from the gut of the earthworm Aporrectodea caliginosa. Int. J. Syst. Evol. Microbiol. 55: 1255-1265 [Abstract] [Full Text]  
• Horn, M. A., Schramm, A., Drake, H. L. (2003). The Earthworm Gut: an Ideal Habitat for Ingested N2O-Producing Microorganisms. Appl. Environ. Microbiol. 69: 1662-1669 [Abstract] [Full Text]