Divergent molecular responses of greater amberjack (Seriola dumerili) to acute salinity stress revealed by comparative transcriptome analysis

Abstract

Greater amberjack (Seriola dumerili) is an important commercial fish for its high growth rate and excellent flesh quality. However, its sensitivity to variations of water salinity poses challenges to the cage culture. In this study, the greater amberjack were reared in the optimum salinity (30 ppt, CK) and undesired regimes (10 and 40 ppt) for 72 hours. The molecular adaptive mechanisms to salinity stress were revealed by the comparative transcriptome analysis for the gills and kidneys. In gills, a total of 445 and 423 differentially expressed genes (DEGs) were identified in 10 and 40 ppt salinity stress groups, respectively. Those DEGs were involved in cartilage and skeletal development, ions transport, and immune response. The major ion secretion and osmoregulation transport proteins gene slc12a2/nkcc1 and cftr expression levels were significantly down-regulated at 10 ppt, but slightly activated at 40 ppt, compared with the control group. The expression changes in response to the Na+, K+ movement, and Cl- ion secretion reduced under the hypo-osmotic exposure and ion excretion boost upon hyper-salinity stress. Meanwhile, the cartilage and skeletal development were enhanced in the gills by hypo- or hyper-salinity stimuli, which is critical for maintaining gill structures and improving respiration and osmoregulation under salinity stress. In kidneys, 600 and 539 DEGs were identified in 10 and 40 ppt groups, respectively. Those DEGs were enriched in oxygen transport, pronephros development, regulation of growth, blood coagulation, ion transmembrane transport, and immune response. While the known renal Na+/Cl– co-transporter gene slc12a3/ncc expression level was significantly down-regulated at 10 ppt, the organic cation transporter 2 gene slc22a2, ammonium transmembrane transport gene rhd and rhag expression levels were overexpressed under the hyper-salinity condition at 40 ppt, contributing to the salts secretion and ammonium transport regulation, to combat the osmotic influx of salts following the drink of seawater and elevated ammonia production upon high salinity stress. These findings advance our knowledge of adaptative mechanisms to the salinity stress and provide theoretical guidance for the optimal breeding mode for the aquaculture of greater amberjack.

Effect of Adding Cortisol and Thyroxin Hormones to the Grass carp “Ctenopharyngodon idella (Val., 1844)” Diets on Some Physiological and Nutritional Parameters During Salt Acclimatization

“…Negative effects were noted on fish growth, reproduction, survival rates, metabolism, and immunity when saline-alkali fluctuations exceeded its osmoregulation capacity (Sultan & Ahmed, 2014;Shi et al, 2023). Furthermore, these variations can have an effect on the performance of fish, the quality of their flesh, and the overall production in the field of aquaculture.…”

“…This is due to the trade-off in resource allocation between energy expended on osmoregulation and growth of energy in the optimal salinity conditions (Liu et al, 2023). However, when fish deviate from both ionic and osmotic homeostasis due to critical salinity conditions, it has the potential to disrupt their energy supply and hormone production (Tsuzuki et al, 2007;Shi et al, 2023).…”

Alternative splicing plays a nonredundant role in greater amberjack (Seriola dumerili) in the adaptation to ambient salinity fluctuations

“…Greater amberjack is an economically important fish that is widely popular for its tasty meat, and it is also a major predator and inhabitant of artificial reefs such as coral reefs and shipwrecks, maintaining the structure and function of these ecosystems (Pereira et al, 2023). It has been widely reported that the growth, development, and physiology of greater amberjack were sensitive to the changes of water salinity, temperature, and seawater pressure (Barany et al, 2021;Navarro-Guillen et al, 2022;Peng et al, 2022;Liu et al, 2023;Ru et al, 2023). Comparative transcriptomic analyses showed that salinity alternations substantially disrupt tissue growth and development, energy metabolism, and immune responses in greater amberjack (Peng et al, 2022;Liu et al, 2023).…”

“…It has been widely reported that the growth, development, and physiology of greater amberjack were sensitive to the changes of water salinity, temperature, and seawater pressure (Barany et al, 2021;Navarro-Guillen et al, 2022;Peng et al, 2022;Liu et al, 2023;Ru et al, 2023). Comparative transcriptomic analyses showed that salinity alternations substantially disrupt tissue growth and development, energy metabolism, and immune responses in greater amberjack (Peng et al, 2022;Liu et al, 2023). Correspondingly, muscle water content, gill and intestinal Na-K-ATPase activity, and growth-related processes were enhanced to combat the adverse impacts (Barany et al, 2021;Liu et al, 2023).…”

“…Salinity fluctuations in seawater would alter the dissolved oxygen level, nutrient concentration, and stratification of the oceans, thereby posting an adverse impact on the respiration, metabolism, reproduction, and even disease immunity of marine organisms (Lehtonen et al, 2016;Guo et al, 2020;Galkanda-Arachchige et al, 2021;Lu et al, 2022;Lacy et al, 2023;Röthig et al, 2023). For example, the increased water salinity was found to disrupt the normal energy allocation, and physiological and metabolic processes of fish, such as grass carp (Ctenopharyngodon idella) and African catfish (Clarias gariepinus), and finally inhibit their growth and survival (Smyth and Elliott, 2016;Zidan et al, 2022;Liu et al, 2023). Moreover, salinity change-induced biodiversity loss of plankton, macroalgae, coral reef, and seagrass may cause trophic collapse of marine ecosystem and lead to drops in fishery yield, which threaten ecosystem functions and food supply to human (Röthig et al, 2023).…”