Transcriptomic responses of juvenile Pacific whiteleg shrimp,Litopenaeus vannamei, to hypoxia and hypercapnic hypoxia

Abstract

Estuarine crustaceans are often exposed to low dissolved O2 (hypoxia) accompanied by elevated CO2 (hypercapnia), which lowers water pH. Acclimatory responses to hypoxia have been widely characterized; responses to hypercapnia in combination with hypoxia (hypercapnic hypoxia) are less well known. Here we used oligonucleotide microarrays to characterize changes in global gene expression in the hepatopancreas of Pacific whiteleg shrimp, Litopenaeus vannamei, exposed to hypoxia or hypercapnic hypoxia for 4 or 24 h, compared with time-matched animals held in air-saturated water (normoxia). Unigenes whose expressions were significantly impacted by treatment and/or time were used to build artificial neural networks (ANNs) to identify genes with the greatest sensitivity in pairwise discriminations between treatments at each time point and between times for each treatment. ANN gene sets that discriminated hypoxia or hypercapnic hypoxia from normoxia shared functions of translation, mitochondrial energetics, and cellular defense. GO terms protein modification/phosphorylation/cellular protein metabolism and RNA processing/apoptosis/cell cycling occurred at highest frequency in discriminating hypercapnic hypoxia from hypoxia at 4 and 24 h, respectively. For 75.4% of the annotated ANN genes, exposure to hypercapnic hypoxia for 24 h reduced or reversed the transcriptional response to hypoxia alone. These results suggest that high CO2/low pH may interfere with transcriptionally based acclimation to hypoxia or elicit physiological or biochemical responses that relieve internal hypoxia. Whether these data reflect resilience or sensitivity of L. vannamei in the face of expanding hypoxic zones and rising levels of atmospheric CO2 may be important to understanding the survival of this and other estuarine species.

Effect of hypercapnic hypoxia and bacterial infection (Vibrio campbellii) on protein synthesis rates in the Pacific whiteleg shrimp,Litopenaeus vannamei

“…There does appear to be some agreement that a change in the capacity for protein synthesis (C s ) is not a major mechanism for reducing protein synthesis rates during hypoxia (24,40,61,84), and that translational efficiencies may play a more central role in facilitating this effect. This has been further supported in L. vannamei by a recent transcriptomic analysis documenting that the expression of hepatopancreas genes associated with translation (along with mitochondrial energetics and cellular defense) was highly sensitive in discriminating between L. vannamei exposed to the same regimes of normoxia, hypoxia, or hypercapnia hypoxia used in this study (74). Modifications in translational efficiency tend to enable changes in protein synthesis rates that are associated with other types of environmental stress (e.g., salinity, temperature, hormones) as well (e.g., 19,43,58,76,86).…”

Transcriptional stress responses to environmental and husbandry stressors in aquaculture species

“…Based on the results from microarray technology, there is a suggestion that high CO 2 /low pH may conflict with transcriptionally based adaptation to hypoxia or excavate physiological or biochemical responses that mitigate internal hypoxia (Rathburn et al . ).…”

“…In certain cases, there is a naturally occurring combination of hypoxia and hypercapnia during the culture of aquatic animals, but the research area is under-investigated. Based on the results from microarray technology, there is a suggestion that high CO 2 /low pH may conflict with transcriptionally based adaptation to hypoxia or excavate physiological or biochemical responses that mitigate internal hypoxia (Rathburn et al 2013).…”

Identification and characterization of nascent polypeptide-associated complex alpha from Chinese mitten crab (Eriocheir sinensis): A novel stress and immune response gene in crustaceans

“…In addition, NAC is required for Caenorhabditis elegans survival of prolonged heat stress [14]. NACA also has been identified as a stress response gene in juvenile Pacific whiteleg shrimp, Litopenaeus vannamei, to hypoxia and hypercapnic hypoxia [15]. Furthermore, NACA has been demonstrated to be a salt stress-responsive protein in Arabidopsis [16], tomato [17] and other plants.…”