Air Exposure Affects Physiological Responses, Innate Immunity, Apoptosis and DNA Methylation of Kuruma Shrimp, Marsupenaeus japonicus

Abstract

Air exposure stress is a common phenomenon for commercial crustacean species in aquaculture and during waterless transportation. However, the antioxidant responses to air exposure discussed in previous studies may be insufficient to present the complexities involved in this process. The comprehensive immune responses, especially considering the immune genes, cell apoptosis, and epigenetic changes, are still unknown. Accordingly, we investigated the multifaceted responses of Marsupenaeus japonicus to air exposure. The results showed that the expression profiles of the apoptosis genes (e.g., IAP, TXNIP, caspase, and caspase-3) and the hypoxiarelated genes (e.g., hsp70, hif-1α, and HcY) were all dramatically induced in the hepatopancreas and gills of M. japonicus. Heart rates, T-AOC (total antioxidant capacity) and lactate contents showed time-dependent changes upon air exposure. Air exposure significantly induced apoptosis in hepatopancreas and gills. Compared with the control group, the apoptosis index (AI) of the 12.5 h experimental group increased significantly (p < 0.05) in the hepatopancreas and gills. Most individuals in the experimental group (EG, 12.5 h) had lower methylation ratios than the control group (CG). Air exposure markedly reduced the full-methylation and total-methylation ratios (31.39% for the CG and 26.46% for the EG). This study provided a comprehensive understanding of the antioxidant responses of M. japonicus considering its physiology, innate immunity, apoptosis, and DNA methylation levels, and provided theoretical guidance for waterless transportation.

Molecular Identification of Anion Exchange Protein 3 in Pacific White Shrimp (Litopenaeus vannamei): mRNA Profiles for Tissues, Ontogeny, Molting, and Ovarian Development and Its Potential Role in Stress-Induced Gill Damage

“…Tissue apoptosis is normally induced by exposure to environmental stresses in aquatic animals such as fish (AnvariFar et al, 2017). Similar phenomena have also been reported in crustaceans; for example, ammonia exposure, air exposure, and cold shock may induce apoptosis in the hepatopancreas of L. vannamei (Chang et al, 2009;Liang et al, 2016;Wang et al, 2020). In this study, we demonstrated that exposure to water with high or low acidity and high or low salinity significantly increased the number of apoptotic cells in the gills of L. vannamei.…”

“…TUNEL assays and DAPI staining were conducted to detect gill tissue damage under multiple stresses according to a previous description ( Wang et al, 2020 ). The number of apoptotic cells in the gills was determined using the in situ Cell Death Detection Kit (Roche, United States) following the manufacturer’s instructions.…”

Recent advances in crustacean genomics and their potential application in aquaculture

“…194,195 In addition, DNA methylation and many histone modifications have been identified in a number of crustaceans, including shrimp and crabs. [196][197][198] In summary, more efforts are needed to promote the application of pan-genomics, 3D genomics, and epigenomics to crustacean research. The application of genomic resources in the genetic breeding of farmed crustaceans is mainly concentrated on shrimp and crabs.…”

“…Epigenomic analyses have been performed in some crustaceans, e.g., the marbled crayfish and Daphnia pulex 194,195 . In addition, DNA methylation and many histone modifications have been identified in a number of crustaceans, including shrimp and crabs 196–198 . In summary, more efforts are needed to promote the application of pan‐genomics, 3D genomics, and epigenomics to crustacean research.…”

Epigenetic Modulations for Prevention of Infectious Diseases in Shrimp Aquaculture

“…Furthermore, alterations in water quality parameters, such as ammonia/nitrate levels, and exposure to environmental pollutants can instigate oxidative stress and potentially inflict damage to DNA in crustaceans, thereby potentially modulating epigenetic changes [ 188 , 189 , 190 ]. Additionally, air availability has been shown to influence DNA methylation patterns in kuruma shrimps, coinciding with changes in apoptosis and physiological responses [ 191 ]. Moreover, feeding regimes, entailing carefully devised plans encompassing diet composition, nutrient intake, and schedule, can exert significant impacts on the epigenetic changes associated with shrimp immunity and defense functions.…”