Nitrous oxide emission by aquatic macrofauna

Abstract

A large variety of aquatic animals was found to emit the potent greenhouse gas nitrous oxide when nitrate was present in the environment. The emission was ascribed to denitrification by ingested bacteria in the anoxic animal gut, and the exceptionally high N2O-to-N2 production ratio suggested delayed induction of the last step of denitrification. Filter-and deposit-feeding animal species showed the highest rates of nitrous oxide emission and predators the lowest, probably reflecting the different amounts of denitrifying bacteria in the diet. We estimate that nitrous oxide emission by aquatic animals is quantitatively important in nitraterich aquatic environments like freshwater, coastal marine, and deep-sea ecosystems. The contribution of this source to overall nitrous oxide emission from aquatic environments might further increase because of the projected increase of nitrate availability in tropical regions and the numeric dominance of filter-and depositfeeders in eutrophic ecosystems.aquatic animals ͉ eutrophication ͉ sediment ͉ gut microbiology ͉ denitrification

Nitrous oxide production associated with coastal marine invertebrates

“…The specific in situ conditions of the earthworm gut, including anoxia and high concentrations of easily degradable organic carbon, as well as nitrate or nitrite, stimulate the activity of ingested N 2 O-producing soil bacteria (Drake et al 2006). A similar mechanism has been suggested for freshwater invertebrates, whose N 2 O emission is largely explained by their preferred diet: filter-and deposit-feeders show high, shredders and grazers intermediate, and predators very low N 2 O emission rates (Stief et al 2009). This suggests that N 2 O emission is caused by bacteria that are coingested with the food taken up by freshwater invertebrates.…”

“…-1 h -1 was reported (Stief et al 2009). In addition to the higher average rate, the N 2 O emission potential of marine invertebrates is apparently influenced by species-specific traits (i.e.…”

“…Besides the microbial N 2 O production in soils, sediments, and water bodies, N 2 O is also emitted by earthworms and freshwater invertebrates (Karsten & Drake 1997, Drake & Horn 2007, Stief et al 2009). This animal-associated N 2 O production is due to the denitrification activity of ingested bacteria in the anoxic gut.…”

“…This suggests that N 2 O emission is caused by bacteria that are coingested with the food taken up by freshwater invertebrates. N 2 O emission rates of both terrestrial and freshwater invertebrates increase with nitrate and temperature and decrease with oxygen availability, indicating the important role of these environmental factors for gut denitrification (Karsten & Drake 1997, Matthies et al 1999, Stief et al 2009.…”

Indirect control of the intracellular nitrate pool of intertidal sediment by the polychaete Hediste diversicolor

“…Conversely, macrofauna that feed on microphytobenthos may cause the lysis of nitrate-storing cells in the gut (Smith et al 1996). Denitrifying bacteria in the gut can use nitrate leaking out of the lysing microalgal cells and produce nitrous oxide and dinitrogen gas which are emitted from the animal (Stief et al 2009, Heisterkamp et al 2010. Nitrate that is not used in the gut will be excreted and can be used by sediment bacteria in the immediate surroundings of macrofauna burrows as possible hotspots of nitrate respiration.…”