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Physiological and transcriptomic analyses reveal the immune and metabolic responses in gills of rainbow trout (Oncorhynchus mykiss) under moderate and severe hypoxia stress

ABSTRACT: Rainbow trout (Oncorhynchus mykiss), an important economically fish with high food value in China, is very sensitive to hypoxia. The gills are the first tissue to be attacked after hypoxia stress. However, the regulatory mechanisms in gills of rainbow trout to moderate and severe hypoxia stress are unclear. In this study, we determined the changes of biochemical parameters and gene expression in gills of rainbow trout during different periods of hypoxia (4, 8, 12, 24 h, and 1 month) and reoxygenation for 24 h, and analyzed the tissue and transcriptomic changes under moderate hypoxia for 12 h (Tm12G) and severe hypoxia for 12 h (Ts12G) compared with control (CG). The results showed that gill lamellae were bent and ILCM was reduced in the Tm12G group, while this phenomenon was more pronounced in the Ts12G group. At one month of hypoxia, we found that the gill lamellae epithelium was detached. Based on biochemical parameters and transcriptomic analysis, we found that the antioxidant and immune responses were activated, and glucose metabolism, lipid metabolism, and amino acid metabolism were enhanced, however, vitamin metabolism was suppressed under moderate hypoxia stress. Antioxidant and immune responses were activated, and glucose metabolism, lipid metabolism, and amino acid metabolism were enhanced, and nucleotide metabolism also was activated under severe hypoxia stress. From the analysis of gene expression pattern, we found that the expression of hsp90a, tnf, caspase3, mgst1, fih1, hif1a, ddit4, and egln3 showed a tendency to increase and then decrease and recovered after reoxygenation under moderate and severe hypoxia stress. Except for mgst1, the expression of other genes was significantly higher than the control at 12 h of stress. Under hypoxia stress, antioxidant and metabolic responses were first elevated and then decreased with time, and metabolic and immune pathways were activated, which coordinated with each other in response to hypoxia stress. These results provide basic information for an in-depth investigation of the physiological and molecular mechanisms in gills of rainbow trout under hypoxia stress.

ORGANISM(S): Oncorhynchus mykiss

PROVIDER: GSE285417 | GEO | 2024/12/28

REPOSITORIES: GEO

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Project description:The frequency of fish encountering hypoxia has risen dramatically as global warming and water pollution intensify, posing a serious threat to survival. Rainbow trout (Oncorhynchus mykiss), which is an economically important fish worldwide, belongs to a typical hypoxia-sensitive fish. However, little is known about the response mechanisms employed by rainbow trout to hypoxia stress. In this study, we systematically analyzed the changes of liver biochemical parameters in rainbow trout exposed to moderate hypoxic conditions (DO: 4.5 ± 0.1 mg/L) for different durations (4, 8, 12, 24 h and 1 month) and 12 h and 24 h reoxygenation, and histologic and transcriptome (lncRNA, miRNA and mRNA) under hypoxia stress for 12 h (Tm12L) and 1 month (TmlL) compared with control, and the interaction between LOC110520201, miR-2188-y and sod1 was verified by dual-luciferase reporter, overexpression and silencing assays. Histological observations revealed that liver suffered severe damage in Tm12L but not in TmlL. Integrating biochemical parameters and mRNA expression profiles, we found that exposure to short-term hypoxia stress resulted in enhanced immune response, aerobic and anaerobic glycolysis, gluconeogenesis and lipid metabolism. In TmlL, increased anaerobic glycolysis and decreased aerobic glycolysis were observed, and antioxidant and immune capacity has returned to normal. Additionally, several key hypoxia-related genes (epo, vegfc, epor, sod1, ppara, foxo1a, gk, dusp1, nlrc3 and nlrp3) and ceRNA regulatory networks were identified from 2711 differentially expressed (DE) mRNAs, 575 DElncRNAs and 395 DEmiRNAs, including LOC110520201-miR-2188-y-sod1, LOC110533332-miR-144-y-vegfc, LOC110526066-miR-465-x-ppara and LOC110535032-miR-743-y-nlrp3. The analysis of expression patterns in liver and rainbow trout liver cells treated with hypoxia suggested that changes in LOC110520201, miR-2188-y and sod1 showed a ceRNA regulatory relationship. Further experiments demonstrated that sod1 is a target of miR-2188-y, and LOC110520201 silencing increased the expression of miR-2188-y and inhibited sod1 expression. These results facilitated our understanding of the molecular mechanisms of hypoxia response in rainbow trout and provided genetic resources for breeding hypoxia-tolerant varieties.

Project description:Hypoxia negatively affects the behavior, growth, reproduction, and survival of fish, causing serious economic losses to aquaculture. Rainbow trout (Oncorhynchus mykiss), an important economic fish worldwide, belongs to a hypoxia-sensitive fish species. However, the regulatory mechanisms of miRNAs under hypoxia stress response of rainbow trout remains unclear. In this study, rainbow trout were subjected to hypoxia stress (DO: 3.5 mg/L) for 3 h (H3h_L), 12 h (H12h_L), 24 h (H24h_L) and 3 h reoxygenation (R3h_L) to systemically evaluate the changes of miRNA expression profiles in liver, and the functions of sha-miR-92a_L+2R+4 were investigated. We found 17, 144, 57 and 55 differentially expressed (DE) miRNAs in H3h_L vs. control (N_L), H12h_L vs. N_L, H24h_L vs. N_L and R3h_L vs. N_L comparisons, respectively. Enrichment analysis revealed that the targets of these DE miRNAs were significantly enriched in HIF signaling pathway, VEGF signaling pathway, FoxO signaling pathway and glycolysis/gluconeogenesis. Through miRNA-mRNA nteraction and weighted gene co-expression network analysis (WGCNA), five key DE miRNAs (sha-miR-92a_L+2R+4, ssa-miR-128-3p, ssa-miR-101b-3p_R+1, ola-miR-199a-5p_R+2 and tni-miR-199_1ss18CG) were identified, which can target at least two hypoxia-responsive genes, such as vegfaa, ho, glut1a and junb. Functional analysis found that sha-miR-92a_L+2R+4 directly regulated vegfaa expression by targeting its 3′-UTR, overexpression of sha-miR-92a_L+2R+4 significantly decreased vegfaa expression in rainbow trout liver cells, while opposite results were obtained after transfection of sha-miR-92a_L+2R+4 inhibitor. Furthermore, overexpression of sha-miR-92a_L+2R+4 promoted rainbow trout liver cell proliferation and inhibited apoptosis. These results deepen our understanding of the crucial roles of miRNAs under hypoxia stress in rainbow trout, and provide valuable information for further studying the regulatory mechanisms of key hypoxia-responsive miRNAs and breeding hypoxia-tolerant rainbow trout species.

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Physiological and transcriptomic analyses reveal the immune and metabolic responses in gills of rainbow trout (Oncorhynchus mykiss) under moderate and severe hypoxia stress

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