Spleen transcriptome analysis reveals the immune molecular responses to hypohaline or hyperhaline environments in spotted scat (Scatophagus argus)

Abstract

Salinity, an important environmental factor, fluctuates frequently and violently in coastal areas, and its dramatic changes tend to have profound effects on the immune function of teleosts. The spotted scat (Scatophagus argus) can tolerate a wide range of salinity fluctuations. However, little is known about its immune response in low and high salinity environments. To elucidate the molecular immune response, the spleen transcriptome of spotted scat was analyzed by RNA sequencing (RNA-seq) after 22 d of culture in water at 5 ppt salinity (low salinity group, LS), 25 ppt salinity (control group, Ctrl), and 35 ppt salinity (high salinity group, HS). RNA-Seq revealed that 1853 and 3554 DEGs were significantly altered by adaptation to low and high salinity, respectively. In addition, 957 genes were co-enriched in the HS and LS. KEGG analysis showed that the focal adhesion, phagosome, ECM-receptor interaction and cytokine-cytokine receptor interaction pathways were significantly enriched in both the Ctrl vs. LS and Ctrl vs. HS. These pathways are involved in immune regulation. RNA-seq showed that genes related to the immune system (ighm, tsp1, sugt1 and hsp90α1), signaling and interaction (pdgfa, pdgfb, mpl, lamb1, itga2, itga3) and cell community (rac3, flna and plk3r3) were significantly downregulated in both hypohaline and hyperhaline environments. Further analysis showed that activation of the splenic NOD-like receptor signaling pathway and the innate immune system occurred in hypersaline but not in hypohaline environments. Salinity stress, particularly high salinity stress, may reduce immunity by limiting the function of the splenic phagosome, reducing resistance to bacterial adhesion, reducing the immune response to pathogens, reducing cell adhesion ability and, and reducing antimicrobial immunity in spotted scat. Evaluation of immune-related responses to salinity fluctuations could provide insight into the immune status of immune organs and the selection of appropriate salinity levels for cultured coastal marine fish.