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Background T. fasciatus ( Takifugu fasciatus ) faces the same problem as most warm water fish: the water temperature falls far below the optimal growth temperature in winter, causing a massive death of T. fasciatus and large economic losses. Understanding of the cold-tolerance mechanisms of this species is still limited. Integrated application of multi-omics research can provide a wealth of information to help us improve our understanding of low-temperature tolerance in fish. Results To gain a comprehensive and unbiased molecular understanding of cold-tolerance in T. fasciatus , we characterized mRNA-seq and metabolomics of T. fasciatus livers using Illumina HiSeq 2500 and UHPLC-Q-TOF MS. We identified 2544 up-regulated and 2622 down-regulated genes in the liver of T. fasciatus . A total of 40 differential metabolites were identified, including 9 down-regulated and 31 up-regulated metabolites. In combination with previous studies on proteomics, we have established an mRNA-protein-metabolite interaction network. There are 17 DEMs (differentially-expressed metabolites) and 14 DEGs-DEPs (differentially co-expressed genes and proteins) in the interaction network that are mainly involved in fatty acids metabolism, membrane transport, signal transduction, and DNA damage and defense. We then validated a number of genes in the interaction network by qRT-PCR. Additionally, a number of SNPs (single nucleotide polymorphisms) were revealed through the transcriptome data. These results provide key information for further understanding of the molecular mechanisms of T. fasciatus under cold stress. Conclusion The data generated by integrated application of multi-omics can facilitate our understanding of the molecular mechanisms of fish response to low temperature stress. We have not only identified potential genes and SNPs involved in cold tolerance, but also show that some nutrient metabolites may be added to the diet to help the overwintering of T. fasciatus .

In the present study, the complete mitochondrial DNA sequence of the hybrid from Takifugu fasciatus (♀) × T. flavidus (♂) was sequenced and characterized. The genome sequence was 16 443 bp in size, and the gene order and contents were identical with those of congeneric species in the genus Takifugu. Comparing with the complete mitochondrial genome of its parents, the hybrid of T. fasciatus (♀) × T. flavidus (♂) was consistent with a maternal inheritance. All the initiation codons of protein-coding genes are ATG, except for COX1 that begins with GTG. The complete mitogenome of the hybrid of T. fasciatus (♀) × T. flavidus (♂) provides an important dataset for the exploration of mitochondrial inheritance mechanism.

Background: Heat shock proteins (HSPs) play crucial roles in response to temperature changes and biotic stresses. However, the HSP gene family in the pufferfish (Takifugu fasciatus) herring has not been comprehensively investigated. Methods and Results: This study presents a systematic analysis of the HSP70 and HSP90 gene families in T. fasciatus, focusing on gene characterization, conserved structural domains, molecular evolutionary history, and expression patterns of the HSP gene family under stress conditions. The findings reveal that 16 HSP genes are evolutionarily conserved, while hspa4 and hsp90aa appear specific to teleost fish. HSP genes exhibit widespread expression across 11 examined tissues, with most demonstrating high expression levels in the heart, brain, and liver. Furthermore, T. fasciatus was subjected to cryogenic and biotic stresses, revealing distinct expression patterns of HSPs under various stress conditions. The response of HSPs to cold stress and Aeromonas hydrophila infection was sustained. In contrast, gene expression of HSPs significantly changed only in the pre-infection period following Ichthyophthirius multifiliis infection, gradually returning to normal levels in the later stages. Conclusions: These experimental results provide a foundation for further in-depth investigations into the characteristics and functions of HSPs in T. fasciatus.

Takifugu fasciatus is an aquaculture species with high economic value. In recent years, problems such as environmental pollution and inbreeding have caused a serious decline in T. fasciatus germplasm resources. In this study, a high-density genetic linkage map was constructed by whole-genome resequencing. The map consists of 4891 bin markers distributed across 22 linkage groups (LGs), with a total genetic coverage of 2381.353 cM and a mean density of 0.535 cM. Quantitative trait locus (QTL) localization analysis showed that a total of 19 QTLs associated with growth traits of T. fasciatus in the genome-wide significance threshold range, distributed on 11 LGs. In addition, 11 QTLs associated with cold tolerance traits were identified, each scattered on a different LG. Furthermore, we used QTL localization analysis to screen out three candidate genes ( IGF1 , IGF2 , ADGRB ) related to growth in T. fasciatus . Meanwhile, we screened three candidate genes ( HSP90 , HSP70 , and HMGB1 ) related to T. fasciatus cold tolerance. Our study can provide a theoretical basis for the selection and breeding of cold-tolerant or fast-growing T. fasciatus.

During migration, anadromous fish may encounter the effects of temperature and salinity of the water. In this study, we examined the effects of cold stress (25, 21, 17, and 13 °C) and salinity stress (20, 10, and 0 ‰) on morphology, enzyme activity, and gene expression level in the gills sampled from river pufferfish (Takifugu fasciatus). This environmental bifactor stress experiment suggested that the activities of catalase, glutathione peroxidase and total superoxide dismutase, as well as the expression of the sod2, hsp90, and cirp genes, increased with decreasing temperature. Among them, cirp reached its peak expression level before individuals experienced the lowest temperature. The osmosis-related genes nka, ncc, nkcc and cftr, all showed an increasing trend with increasing salinity and decreasing temperature. When cold and salinity stress were enhanced, apoptosis-related genes bcl-2, caspase-3 and caspase-9 promoted apoptosis through downregulation, up-regulation, and up-regulation, respectively. The study of the gill morphology showed that an increase in salinity or a decrease in temperature mainly leads to serious vacuolar lesions in the gill filaments. The results also showed moderate salinity (10 ‰) may alleviate the gill stress responses caused by low temperature. This research exhibited the primary molecular responses of the anadromous fish T. fasciatus under cold and salinity challenges, which could serve as a valuable reference for studying the responses of migratory fish to environmental changes.

Skin sensitivity is increasingly prevalent, necessitating new therapeutic agents. This study screened multifunctional peptides from Takifugu fasciatus skin for transient receptor potential vanilloid 1 (TRPV1)-inhibitory and anti-inflammatory activities and investigated their mechanisms in alleviating sensitive skin (SS). A low-molecular-weight hydrolysate was prepared through enzymatic hydrolysis of T. fasciatus skin, followed by ultrafiltration, with subsequent peptide identification performed using nano-HPLC-MS/MS and molecular docking-based virtual screening. Among 20 TRPV1-antagonistic peptides (TFTIPs), QFF (T10), LDIF (T14), and FFR (T18) exhibited potent anti-inflammatory effects in (lipopolysaccharide) LPS-induced RAW 264.7 macrophages. T14 showed the strongest TRPV1 inhibition; T14 (200 μM) inhibited Ca2⁺ in capsaicin-stimulated HaCaT cells by 73.1% and showed stable binding in molecular docking, warranting further analysis. Mechanistic studies revealed that T14 suppressed NF-κB signaling by downregulating p65 protein expression, thereby reducing pro-inflammatory cytokine secretion (G-CSF, GM-CSF, ICAM-1, IL-6, TNF-α) in RAW 264.7 cells. Additionally, T14 (400 μM) inhibited ET-1 in LPS-stimulated endothelial cells by 75.0%; ICAM-1 reached 49.0%. Network pharmacology predicted STAT3, MAPK3, SPHK1, and CTSB as key targets mediating T14’s effects. These study findings suggest that T14 may be a promising candidate for skincare applications targeting SS.

Hypoxia frequently occurs in aquatic ecosystem, which is influenced by salinity, water temperature, weather, and surface water runoff. In order to shed further light on the evolutionary and adaptive mechanisms in fish under hypoxic condition, the impact of acute hypoxia (1.63 ± 0.2 mg/L) and reoxygenation (7.0 ± 0.3 mg/L) on oxygen sensors, energy metabolism, and hematological indices was evaluated in Takifugu fasciatus. Data from transcriptional level analysis show that the expressions of genes related to oxygen sensors (HIF-1α, PHD2, and VHL) were upregulated in the brain and liver under hypoxia and recovered under reoxygenation. The upregulation of GLUT2, VEGF-A, and EPO in conjugation with VEGF-A protein and hematological indices conferred the rapid adjustments of cellular glucose uptake and blood oxygen-carrying capacities in pufferfish. Higher levels of glycolysis-related mRNAs (HK, PGK1, and PGAM2), HK activity, and proteins (PGK1 and PGAM2) were detected in the brain and liver under hypoxic condition compared with control. Interestingly, the expression of MDH1 at the mRNA, enzyme activity, and protein levels was significantly increased in the brain at 0 or 2 h and in the liver at 8 h under hypoxic condition. In addition, although the enzyme activity and mRNA expression of LDH in the brain were not significantly changed, a persistent upregulation was observed in the liver during hypoxia exposure. This study demonstrated that pufferfish could counterpoise the energetic demands and hematological functional properties evoked by oxygen sensors after hypoxia. Our findings provided new insights into the molecular regulatory mechanism of hypoxia in pufferfish.

17α-methyltestosterone (17α-MT) is an emerging pollutant, which is harmful to the endocrine system and reproduction of fish. We investigated the effects of different concentrations of 17α-MT (0, 5, 30, 60, and 100 mg/kg) on endoplasmic reticulum stress (ERS) and apoptosis in the liver of Takifugu fasciatus . Results show that: (1) with the increase of 17α-MT treatment concentration, liver transaminases (alanine aminotransferase; aspartate aminotransferase) and the mRNA expression of ERS marker genes (glucose-regulated protein 78; calreticulin) of T. fasciatus were significantly increased compared with the control group ( P <0.05); (2) the activity of succinate dehydrogenase (SDH), Caspase3 and Caspase9 in the liver of T. fasciatus increased with the increase of 17α-MT concentration compared with the control group ( P <0.05); (3) by using 4-phenylbutyricacid (4-PBA) inhibitors to stimulate ERS through in vitro experiments, the expression of ERS and apoptosis-related genes significantly decreased ( P <0.05), and the apoptosis rate of T. fasciatus hepatocytes was significantly inhibited ( P <0.05) under 17α-MT treatment. This study confirmed that ERS played an important role in the induction of apoptosis in the hepatocytes of T. fasciatus , which enriched the ecotoxicological information of environmental androgens.

Lipopolysaccharides (LPS) and salinity are important variables in aquatic environments. High concentration of LPS and large changes in salinity seriously threat the survival of a variety of organisms, including fish. To reveal the effects of salinity and LPS on a fish immune response, we measured the immune-related parameters (total leukocyte count, total serum protein, albumin and globulin concentrations, complement C3 concentration, and lysozyme activity) and genes (the expressions of TNF-α, IL-1β, and SOCS1–3 at the mRNA and protein levels) of juvenile Takifugu fasciatus exposed to phosphate buffered saline (PBS) or LPS (25 μg mL−1) under different salinities (0, 15, and 30 ppt) for 24 h. Changes in key immunological indicators suggested that the LPS challenge induced considerable damage to T. fasciatus, whereas an increase in salinity mitigated the harmful effects. Moreover, although the immune responses in blood and other selected tissues (gill and kidney) were suppressed with an increase in salinity, the increased response in liver in saltwater enabled T. fasciatus to conquer large salinity variation during migration. The appropriate addition of salts appeared to be a sensible strategy to mitigate LPS-induced toxicity in the aquaculture of T. fasciatus.

Hypoxia seriously affects the innate immune system of fish. However, the roles of suppressor of cytokine signaling (SOCS), pivotal anti-inflammatory genes, in response to hypoxia/reoxygenation remain largely unexplored. The primary objective of this study was to elucidate the function of SOCS genes under acute hypoxia and reoxygenation in pufferfish (Takifugu fasciatus). In the present study, SOCS1, 2 and 3 were identified in T. fasciatus referred to as TfSOCS1, 2 and 3. Then, qRT-PCR and western blot analysis were employed to assess their expressions at both the mRNA and protein levels. Tissue distribution demonstrated that the three SOCS genes were predominantly distributed in gill, brain and liver. Under hypoxia challenge (1.63 ± 0.2 mg/L DO for 2, 4, 6 and 8 h), the expressions of TfSOCS1 and 3 in brain and liver at the mRNA and protein levels were significantly decreased, while their expressions showed an opposite trend in gill. Different from the expressions of TfSOCS1 and 3, the expression of TfSOCS2 was inhibited in gill, along with its increased expression in brain and liver. After normoxic recovery (7.0 ± 0.3 mg/L of DO for 4 and 12 h), most of TfSOCS genes were significantly altered at R4 (reoxygenation for 4 h) and returned to the normal level at R12 (reoxygenation for 12 h). SOCS genes played vital roles in response to hypoxia/reoxygenation challenge. Our findings greatly strengthened the relation between innate immune and hypoxia stress in T. fasciatus.