Direct Nitrous Oxide Emission from the Aquacultured Pacific White Shrimp (Litopenaeus vannamei)

Abstract

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 (N 2 O) at an average rate of 4.3 nmol N 2 O/individual ؋ h, which is 1 to 2 orders of magnitude higher than previously measured N 2 O emission rates for free-living aquatic invertebrates. Dissection, incubation, and inhibitor experiments with specimens from a shrimp farm in Germany indicated that N 2 O 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 (N 2 ) and N 2 O 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 N 2 O accumulation that outlasted the gut passage time. Shrimp-associated N 2 O production was estimated to account for 6.5% of total N 2 O production in the shrimp farm studied here and to contribute to the very high N 2 O supersaturation measured in the rearing tanks (2,099%). Microbial N 2 O production directly associated with aquacultured animals should be implemented into life cycle assessments of seafood production. IMPORTANCEThe most widely used shrimp species in global aquaculture, Litopenaeus vannamei, is shown to emit the potent greenhouse gas nitrous oxide (N 2 O) at a particularly high rate. Detailed experiments reveal that N 2 O 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 N 2 O as an intermediate and dinitrogen (N 2 ) gas as an end product. The N 2 O/N 2 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 N 2 O emission from aquaculture facilities.

Evaluación del efecto de Bacillus firmus C101 en el crecimiento de poslarvas de Litopenaeus vannamei Boone (camarón blanco) y Brachionus plicatilis s.s. Müller (rotífero)

“…Some studies of the effect of the administration of bacteria of the genus Bacillus sp. in white shrimp (Litopenaeus vannamei) of different stages El crecimiento, la resistencia a cambios de temperatura, salinidad, y las condiciones fisiológicas del tracto gastrointestinal (TGI) de los organismos, el cual es ligeramente alcalino (pH ~ 8,0) y con una alta concentración de sales biliares (Heisterkamp et al, 2016), son características que debe cumplir un buen candidato a probiótico (Balcázar et al, 2006;Reddy et al, 2018). De acuerdo con lo anterior, el perfil fisiológico de B. firmus C101 y el hecho de que algunas cepas de B. firmus pueden adherirse y formar biopelículas en el tracto intestinal de organismos acuáticos (Kesarcodi-Watson et al, 2008) sugieren que existe una alta probabilidad de colonización del TGI de las poslarvas de camarón blanco y una alta probabilidad de supervivencia bajo estas condiciones, por lo que en futuras investigaciones sería pertinente efectuar un análisis de la diversidad microbiana intestinal con técnicas independientes de cultivo.…”

“…Adicionalmente, el perfil bioquímico de B. firmus C101 sugiere una alta actividad enzimática de hidrolasas como las lipasas/esterasas, quimotripsinas y fosfatasas, las Growth, resistance to changes in temperature, salinity, and the physiological conditions of the gastrointestinal tract (TGI) of organisms, which is slightly alkaline (pH ~ 8.0) and with a high concentration of bile salts (Heisterkamp et al, 2016), are characteristics that a good probiotic candidate must meet (Balcázar et al, 2006;Reddy et al, 2018). Following the above, the physiological profile of B. firmus C101 and the fact that some strains of B. firmus can adhere and form biofilms in the intestinal tract of aquatic organisms (Kesarcodi-Watson et al, 2008) suggest that there is a high probability of TGI colonization of white shrimp postlarvae and a high probability of survival under these conditions, therefore it would be pertinent in future researches to carry out analyzes of intestinal microbial diversity with independent culture techniques.…”

Feeding-related controls on microbial nitrogen cycling associated with the Arctic marine copepod Calanus hyperboreus

“…The gut microbial community itself is involved in creating these microenvironmental conditions. First, the aerobic activity of heterotrophic microorganisms in the food promotes gut anoxia (Tang et al 2011, Heisterkamp et al 2016, which triggers a shift to anaerobic metabolism in many microorganisms ingested by aquatic invertebrates (Stief et al 2009, Heisterkamp et al 2010. Second, the microbial community of the copepod gut contributes to the solubilization of organic food particles through exoenzyme activities (Lawrence et al 1993).…”

“…Schreiber et al 2010, Marchant et al 2017. Aerobic denitrification is facilitated by the constitutive expression of denitrification genes independent of the ambient O 2 level and is thus advantageous in environments with fluctuating O 2 levels, as may be the case for the guts of aquatic invertebrates (Tang et al 2011, Heisterkamp et al 2016.…”

Proteomic Responses Under Cold Stress Reveal Unique Cold Tolerance Mechanisms in the Pacific White Shrimp (Litopenaeus vannamei)

“…Abiotic stresses also considerably influence the aquaculture of these organisms. These stresses include low temperatures, which can cause persistent effects on fish muscle ( Schnurr et al, 2014 ), and acute ammonia stress, which can lead to the death of the Pacific white shrimp ( Heisterkamp et al, 2016 ; Lu et al, 2016 ).…”