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Applied and Environmental Microbiology, April 2009, p. 1852-1859, Vol. 75, No. 7
0099-2240/09/$08.00+0     doi:10.1128/AEM.02745-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

In Situ Hydrogen and Nitrous Oxide as Indicators of Concomitant Fermentation and Denitrification in the Alimentary Canal of the Earthworm Lumbricus terrestris{triangledown}

Pia K. Wüst, Marcus A. Horn, and Harold L. Drake*

Department of Ecological Microbiology, University of Bayreuth, 95445 Bayreuth, Germany

Received 2 December 2008/ Accepted 23 January 2009

The earthworm gut is a unique microzone in aerated soils that has been proposed to selectively stimulate ingested soil microorganisms by its in situ conditions, which include anoxia, high water content, a near-neutral pH, and high concentrations of organic compounds. The central objective of this study was to resolve potential links between in situ conditions and anaerobic microbial activities during the gut passage of Lumbricus terrestris. Both H2 and N2O were emitted by living earthworms, and in situ microsensor analyses revealed both H2 and N2O in the O2-free gut center. The highest H2 concentrations occurred in foregut and midgut regions, whereas the highest N2O concentrations occurred in crop/gizzard and hindgut regions. Thus, H2-producing fermentations were more localized in the foregut and midgut, whereas denitrification was more localized in the crop/gizzard and hindgut. Moisture content, total carbon, and total nitrogen were highest in the foregut and decreased from the anterior to posterior end of the gut. Nitrite, ammonium, and iron(II) concentrations were highest in the crop/gizzard and decreased from the anterior to posterior end of the alimentary canal. Concentrations of soluble organic compounds were indicative of distinct fermentation processes along the alimentary canal, with maximal concentrations of organic acids (e.g., acetate and butyrate) occurring in the midgut. These findings suggest that earthworms (i) contribute to the terrestrial cycling of carbon and nitrogen via anaerobic microbial activities in the alimentary canal and (ii) constitute a mobile source of reductant (i.e., emitted H2) for microbiota in aerated soils.


* Corresponding author. Mailing address: Department of Ecological Microbiology, University of Bayreuth, 95445 Bayreuth, Germany. Phone: (49) (0)921-555640. Fax: (49) (0)921-555793. E-mail: HLD{at}Uni-Bayreuth.De

{triangledown} Published ahead of print on 5 February 2009.


Applied and Environmental Microbiology, April 2009, p. 1852-1859, Vol. 75, No. 7
0099-2240/09/$08.00+0     doi:10.1128/AEM.02745-08
Copyright © 2009, 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]