In Vivo Emission of Dinitrogen by Earthworms via Denitrifying Bacteria in the Gut

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Abstract
Earthworms emit the greenhouse gas nitrous oxide (N 2 O), and ingested denitrifiers in the gut appear to be the main source of this N 2 O. The primary goal of this study was to determine if earthworms also emit dinitrogen (N 2 ), the end product of complete denitrification. When [ 15 N]nitrate was injected into the gut, the earthworms Aporrectodea caliginosa and Lumbricus terrestris emitted labeled N 2 (and also labeled N 2 O) under in vivo conditions; emission of N 2 by these two earthworms was relatively linear and approximated 1.2 and 6.6 nmol N 2 per h per g (fresh weight), respectively. Isolated gut contents also produced [ 15 N]nitrate-derived N 2 and N 2 O under anoxic conditions. N 2 is formed by N 2 O reductase, and acetylene, an inhibitor of this enzyme, inhibited the emission of [ 15 N]nitrate-derived N 2 by living earthworms. Standard gas chromatographic analysis demonstrated that the amount of N 2 O emitted was relatively linear during initial incubation periods and increased in response to acetylene. The calculated rates for the native emissions of N 2 (i.e., without added nitrate) by A. caliginosa and L. terrestris were 1.1 and 1.5 nmol N 2 per h per g (fresh weight), respectively; these emission rates approximated that of N 2 O. These collective observations indicate that (i) earthworms emit N 2 concomitant with the emission of N 2 O via the in situ activity of denitrifying bacteria in the gut and (ii) N 2 O is quantitatively an important denitrification-derived end product under in situ conditions.