TY - JOUR
T1 - Direct nitrous oxide emission from the aquacultured Pacific white shrimp (Litopenaeus vannamei)
AU - Heisterkamp, Ines M.
AU - Schramm, Andreas
AU - de Beer, Dirk
AU - Stief, Peter
PY - 2016/6/14
Y1 - 2016/6/14
N2 - UNLABELLED: The Pacific white shrimp (Litopenaeus vannamei) is widely used in aquaculture, where it is reared at high stocking densities, temperatures, and nutrient concentrations. Here we report that adult L. vannamei shrimp emit the greenhouse gas nitrous oxide (N2O) at an average rate of 4.3 nmol N2O/individual × h, which is 1 to 2 orders of magnitude higher than previously measured N2O emission rates for free-living aquatic invertebrates. Dissection, incubation, and inhibitor experiments with specimens from a shrimp farm in Germany indicated that N2O is mainly produced in the animal's gut by microbial denitrification. Microsensor measurements demonstrated that the gut interior is anoxic and nearly neutral and thus is favorable for denitrification by ingested bacteria. Dinitrogen (N2) and N2O accounted for 64% and 36%, respectively, of the nitrogen gas flux from the gut, suggesting that the gut passage is too fast for complete denitrification to be fully established. Indeed, shifting the rearing water bacterial community, a diet component of shrimp, from oxic to anoxic conditions induced N2O accumulation that outlasted the gut passage time. Shrimp-associated N2O production was estimated to account for 6.5% of total N2O production in the shrimp farm studied here and to contribute to the very high N2O supersaturation measured in the rearing tanks (2,099%). Microbial N2O production directly associated with aquacultured animals should be implemented into life cycle assessments of seafood production.IMPORTANCE: The most widely used shrimp species in global aquaculture, Litopenaeus vannamei, is shown to emit the potent greenhouse gas nitrous oxide (N2O) at a particularly high rate. Detailed experiments reveal that N2O is produced in the oxygen-depleted gut of the animal by bacteria that are part of the shrimp diet. Upon ingestion, these bacteria experience a shift from oxic to anoxic conditions and therefore switch their metabolism to the anaerobic denitrification process, which produces N2O as an intermediate and dinitrogen (N2) gas as an end product. The N2O/N2 production ratio is unusually high in the shrimp gut, because denitrification cannot be fully established during the short gut passage time of food-associated bacteria. Nitrous oxide emission directly mediated by L. vannamei contributes significantly to the overall N2O emission from aquaculture facilities.
AB - UNLABELLED: The Pacific white shrimp (Litopenaeus vannamei) is widely used in aquaculture, where it is reared at high stocking densities, temperatures, and nutrient concentrations. Here we report that adult L. vannamei shrimp emit the greenhouse gas nitrous oxide (N2O) at an average rate of 4.3 nmol N2O/individual × h, which is 1 to 2 orders of magnitude higher than previously measured N2O emission rates for free-living aquatic invertebrates. Dissection, incubation, and inhibitor experiments with specimens from a shrimp farm in Germany indicated that N2O is mainly produced in the animal's gut by microbial denitrification. Microsensor measurements demonstrated that the gut interior is anoxic and nearly neutral and thus is favorable for denitrification by ingested bacteria. Dinitrogen (N2) and N2O accounted for 64% and 36%, respectively, of the nitrogen gas flux from the gut, suggesting that the gut passage is too fast for complete denitrification to be fully established. Indeed, shifting the rearing water bacterial community, a diet component of shrimp, from oxic to anoxic conditions induced N2O accumulation that outlasted the gut passage time. Shrimp-associated N2O production was estimated to account for 6.5% of total N2O production in the shrimp farm studied here and to contribute to the very high N2O supersaturation measured in the rearing tanks (2,099%). Microbial N2O production directly associated with aquacultured animals should be implemented into life cycle assessments of seafood production.IMPORTANCE: The most widely used shrimp species in global aquaculture, Litopenaeus vannamei, is shown to emit the potent greenhouse gas nitrous oxide (N2O) at a particularly high rate. Detailed experiments reveal that N2O is produced in the oxygen-depleted gut of the animal by bacteria that are part of the shrimp diet. Upon ingestion, these bacteria experience a shift from oxic to anoxic conditions and therefore switch their metabolism to the anaerobic denitrification process, which produces N2O as an intermediate and dinitrogen (N2) gas as an end product. The N2O/N2 production ratio is unusually high in the shrimp gut, because denitrification cannot be fully established during the short gut passage time of food-associated bacteria. Nitrous oxide emission directly mediated by L. vannamei contributes significantly to the overall N2O emission from aquaculture facilities.
KW - Aerobiosis
KW - Anaerobiosis
KW - Animals
KW - Aquaculture
KW - Bacteria/metabolism
KW - Denitrification
KW - Gastrointestinal Tract/microbiology
KW - Germany
KW - Nitrous Oxide/metabolism
KW - Penaeidae/metabolism
U2 - 10.1128/AEM.00396-16
DO - 10.1128/AEM.00396-16
M3 - Journal article
C2 - 27129966
SN - 0099-2240
VL - 82
SP - 4028
EP - 4034
JO - Applied and Environmental Microbiology
JF - Applied and Environmental Microbiology
IS - 13
ER -