Association of Earthworm-Denitrifier Interactions with Increased Emission of Nitrous Oxide from Soil Mesocosms Amended with Crop Residue

Abstract

Earthworm activity is known to increase emissions of nitrous oxide (N2O) from arable soils. Earthworm gut, casts, and burrows have exhibited higher denitrification activities than the bulk soil, implicating priming of denitrifying organisms as a possible mechanism for this effect. Furthermore, the earthworm feeding strategy may drive N2O emissions, as it determines access to fresh organic matter for denitrification. Here, we determined whether interactions between earthworm feeding strategy and the soil denitrifier community can predict N2O emissions from the soil. We set up a 90-day mesocosm experiment in which 15N-labeled maize (Zea mays L.) was either mixed in or applied on top of the soil in the presence or absence of the epigeic earthworm Lumbricus rubellus and/or the endogeic earthworm Aporrectodea caliginosa. We measured N2O fluxes and tested the bulk soil for denitrification enzyme activity and the abundance of 16S rRNA and denitrifier genes nirS and nosZ through real-time quantitative PCR. Compared to the control, L. rubellus increased denitrification enzyme activity and N2O emissions on days 21 and 90 (day 21, P = 0.034 and P = 0.002, respectively; day 90, P = 0.001 and P = 0.007, respectively), as well as cumulative N2O emissions (76%; P = 0.014). A. caliginosa activity led to a transient increase of N2O emissions on days 8 to 18 of the experiment. Abundance of nosZ was significantly increased (100%) on day 90 in the treatment mixture containing L. rubellus alone. We conclude that L. rubellus increased cumulative N2O emissions by affecting denitrifier community activity via incorporation of fresh residue into the soil and supplying a steady, labile carbon source