In situ hydrogen and nitrous oxide as indicators of concomitant fermentation and denitrification in the alimentary canal of the earthworm Lumbricus terrestris.
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 H(2) and N(2)O were emitted by living earthworms, and in situ microsensor analyses revealed both H(2) and N(2)O in the O(2)-free gut center. The highest H(2) concentrations occurred in foregut and midgut regions, whereas the highest N(2)O concentrations occurred in crop/gizzard and hindgut regions. Thus, H(2)-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 H(2)) for microbiota in aerated soils.
Wüst
Pia K
PK
Department of Ecological Microbiology, University of Bayreuth, 95445 Bayreuth, Germany.
Horn
Marcus A
MA
Drake
Harold L
HL
D000818:Animals; D002244:Carbon / Q000032:analysis; D002264:Carboxylic Acids / Q000032:analysis; D004064:Digestive System / Q000737:chemistry* / Q000382:microbiology; D005285:Fermentation; D005290:Ferric Compounds / Q000032:analysis; D006859:Hydrogen / Q000032:analysis*; D009566:Nitrates / Q000378:metabolism; D009573:Nitrites / Q000032:analysis; D009584:Nitrogen / Q000032:analysis; D009609:Nitrous Oxide / Q000032:analysis*; D009835:Oligochaeta / Q000737:chemistry* / Q000382:microbiology; D000644:Quaternary Ammonium Compounds / Q000032:analysis
D002264:Carboxylic Acids; D005290:Ferric Compounds; D009566:Nitrates; D009573:Nitrites; D000644:Quaternary Ammonium Compounds; D002244:Carbon; D006859:Hydrogen; D009609:Nitrous Oxide; D009584:Nitrogen