2512002539
  • Open Access
  • Article

Transcriptomic Analysis of Liver Response in Juvenile Yellowfin Tuna (Thunnus albacares) Under Acute Heat Stress

  • Junhua Huang 1,2,3,4,5,   
  • Zhengyi Fu 1,2,3,4,6,   
  • Jing Bai 7,   
  • Zhenhua Ma 1,2,3,4,6,*

Received: 22 Sep 2025 | Revised: 05 Dec 2025 | Accepted: 16 Dec 2025 | Published: 07 Jan 2026

Abstract

Ocean warming driven by climate change has led to an increased frequency of extreme high-temperature events, posing serious threats to marine organisms. Yellowfin tuna (Thunnus albacares), a pelagic species with partial endothermic traits, holds high ecological and economic value but remains highly sensitive to acute thermal stress. In this study, we simulated heatwave conditions in the South China Sea by exposing juvenile yellowfin tuna to 34 °C (high-temperature group, HT) and 28 °C (control group, LT), and analyzed hepatic transcriptomic responses at 6 h and 24 h. A total of 778 and 524 differentially expressed genes (DEGs) were identified at 6 h and 24 h, respectively, with 155 shared DEGs. KEGG enrichment analysis showed that these common DEGs were significantly associated with key pathways such as protein processing in the endoplasmic reticulum, herpes simplex virus 1 infection, and antigen processing and presentation. Clustering analysis revealed that classical stress-response genes, including hspa5, dnajc3a, hspa4l, and hsp90b1, were significantly upregulated under heat stress. Protein–protein interaction (PPI) analysis further confirmed these genes as central hubs within molecular chaperone and protein-folding modules. In contrast, immune-related genes such as MHC1, IFIH1, and KRAB were downregulated and showed weak or no interactions in the network. This study provides molecular insights into the thermal stress response of yellowfin tuna and offers a theoretical basis for the development of heat-resilient breeding strategies and improved aquaculture management.

References 

  • 1.

    Wernberg, T.; Thomsen, M.S.; Burrows, M.T.; et al. Marine Heatwaves as Hot Spots of Climate Change and Impacts on Biodiversity and Ecosystem Services. Nat. Rev. Biodivers. 2025, 1, 461–479. https://doi.org/10.1038/s44358-025-00058-5.

  • 2.

    Moura, M.M.; Dos Santos, A.R.; Pezzopane, J.E.M.; et al. Relation of El Niño and La Niña Phenomena to Precipitation, Evapotranspiration and Temperature in the Amazon Basin. Sci. Total Environ. 2019, 651, 1639–1651. https://doi.org/10.1016/j.scitotenv.2018.09.242.

  • 3.

    Thirumalai, K.; DiNezio, P.N.; Okumura, Y.; et al. Extreme Temperatures in Southeast Asia Caused by El Niño and Worsened by Global Warming. Nat. Commun. 2017, 8, 15531. https://doi.org/10.1038/ncomms15531.

  • 4.

    Li, M.; Xu, Y.; Sun, M.; et al. Impacts of Strong ENSO Events on Fish Communities in an Overexploited Ecosystem in the South China Sea. Biology 2023, 12, 946. https://doi.org/10.3390/biology12070946.

  • 5.

    Reynolds, W.W.; Casterlin, M.E. The Role of Temperature in the Environmental Physiology of Fishes. In Environmental Physiology of Fishes; Springer: Berlin/Heidelberg, Germany, 1980; pp. 497–518.

  • 6.

    Chowdhury, S.; Saikia, S. Oxidative Stress in Fish: A review. J. Sci. Res. 2020, 12, 145–160. https://doi.org/10.3329/jsr.v12i1.41716.

  • 7.

    Chen, Y.; Chen, S.-Q.; Zhang, B.; et al. Effects of Acute High-Temperature on Gill Tissue Structure, Serum Biochemical Indices, Antioxidant Capacity and Liver Transcriptomics of Thamnaconus septentrionalis. J. Therm. Biol. 2025, 129, 104098. https://doi.org/10.1016/j.jtherbio.2025.104098.

  • 8.

    Bard, B.; Kieffer, J.D. The Effects of Repeat Acute Thermal Stress on the Critical Thermal Maximum (CTmax) and Physiology of Juvenile Shortnose Sturgeon (Acipenser brevirostrum). Can. J. Zool. 2019, 97, 567–572. https://doi.org/10.1139/cjz-2018-0157.

  • 9.

    Munday, P.; Kingsford, M.; O’callaghan, M.; et al. Elevated Temperature Restricts Growth Potential of the Coral Reef Fish Acanthochromis polyacanthus. Coral Reefs 2008, 27, 927–931. https://doi.org/10.1007/s00338-008-0393-4.

  • 10.

    Huang, J.; Fu, Z.; Bai, J.; et al. Cold Stress Disrupts Gill Homeostasis in Juvenile Yellowfin Tuna (Thunnus albacares) by Altering Oxidative, Metabolic, and Immune Responses. Mar. Environ. Res. 2025, 107300. https://doi.org/10.1016/j.marenvres.2025.107300.

  • 11.

    Franck, J.P.; Robinson, S.W. Endothermy in Fish: A Remarkable Story of Convergent Evolutionary Adaptation. In Biochemistry of Non-Shivering Thermogenesis in Vertebrates; CRC Press: Boca Raton, FL, USA, 2025; pp. 55–66.

  • 12.

    Muñoz-Abril, L.J. Biology and Connectivity of Yellowfin Tuna in the Eastern Pacific Ocean. Doctoral Dissertation, University of South Alabama, Mobile, AL, USA, 2024.

  • 13.

    Schaefer, K.M.; Fuller, D.W.; Block, B.A. Movements, Behavior, and Habitat Utilization of Yellowfin Tuna (Thunnus albacares) in the Northeastern Pacific Ocean, Ascertained through Archival Tag Data. Mar. Biol. 2007, 152, 503–525. https://doi.org/10.1007/s00227-007-0689-x.

  • 14.

    Jayasundara, N.; Gardner, L.D.; Block, B.A. Effects of Temperature Acclimation on Pacific Bluefin Tuna (Thunnus orientalis) Cardiac Transcriptome. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305, R1010–R1020. https://doi.org/10.1152/ajpregu.00254.2013.

  • 15.

    Fu, Z.; Bai, J.; Ma, Z. Physiological Adaptations and Stress Responses of Juvenile Yellowfin Tuna (Thunnus albacares) in Aquaculture: An Integrative Review. Aquat. Life Ecosyst. 2025, 1, 3.

  • 16.

    Liu, H.; Fu, Z.; Yu, G.; et al. Effects of Acute High-Temperature Stress on Physical Responses of Yellowfin Tuna (Thunnus albacares). J. Mar. Sci. Eng. 2022, 10, 1857. https://doi.org/10.3390/jmse10121857.

  • 17.

    Liu, H.; Yang, R.; Fu, Z.; et al. Acute Thermal Stress Increased Enzyme Activity and Muscle Energy Distribution of Yellowfin Tuna. PLoS ONE 2023, 18, e0289606. https://doi.org/10.1371/journal.pone.0289606.

  • 18.

    Mokhtar, D.M.; Zaccone, G.; Alesci, A.; et al. Main Components of Fish Immunity: An Overview of the Fish Immune System. Fishes 2023, 8, 93. https://doi.org/10.3390/fishes8020093.

  • 19.

    Wang, M.; Xu, G.; Tang, Y.; et al. Investigation of the Molecular Mechanisms of Antioxidant Damage and Immune Response Downregulation in Liver of Coilia nasus Under Starvation Stress. Front. Endocrinol. 2021, 12, 622315. https://doi.org/10.3389/fendo.2021.622315.

  • 20.

    Jia, R.; Du, J.; Cao, L.; et al. Antioxidative, Inflammatory and Immune Responses in Hydrogen Peroxide-Induced Liver Injury of Tilapia (GIFT, Oreochromis niloticus). Fish Shellfish. Immunol. 2019, 84, 894–905. https://doi.org/10.1016/j.fsi.2018.10.084.

  • 21.

    Liu, E.; Zhao, X.; Li, C.; et al. Effects of Acute Heat Stress on Liver Damage, Apoptosis and Inflammation of Pikeperch (Sander lucioperca). J. Therm. Biol. 2022, 106, 103251. https://doi.org/10.1016/j.jtherbio.2022.103251.

  • 22.

    Roychowdhury, P.; Aftabuddin, M.; Pati, M.K. Thermal Stress-Induced Oxidative Damages in the Liver and Associated Death in Fish, Labeo rohita. Fish Physiol. Biochem. 2021, 47, 21–32. https://doi.org/10.1007/s10695-020-00880-y.

  • 23.

    Feidantsis, K.; Georgoulis, I.; Zachariou, A.; et al. Energetic, Antioxidant, Inflammatory and Cell Death Responses in the Red Muscle of Thermally Stressed Sparus aurata. J. Comp. Physiol. B 2020, 190, 403–418. https://doi.org/10.1007/s00360-020-01278-1.

  • 24.

    Sudhagar, A.; Kumar, G.; El-Matbouli, M. Transcriptome Analysis Based on RNA-Seq in Understanding Pathogenic Mechanisms of Diseases and the Immune System of Fish: A Comprehensive Review. Int. J. Mol. Sci. 2018, 19, 245. https://doi.org/10.3390/ijms19010245.

  • 25.

    Liu, Y.; Tian, C.; Yang, Z.; et al. Effects of Chronic Heat Stress on Growth, Apoptosis, Antioxidant Enzymes, Transcriptomic Profiles, and Immune-Related Genes of Hong Kong Catfish (Clarias fuscus). Animals 2024, 14, 1006. https://doi.org/10.3390/ani1407100.

  • 26.

    Long, Y.; Li, L.; Li, Q.; et al. Transcriptomic Characterization of Temperature Stress Responses in Larval Zebrafish. PLoS ONE 2012, 7, e37209. https://doi.org/10.1371/journal.pone.0037209.

  • 27.

    Beemelmanns, A.; Zanuzzo, F.S.; Xue, X.; et al. The Transcriptomic Responses of Atlantic salmon (Salmo salar) to High Temperature Stress Alone, and in Combination with Moderate Hypoxia. BMC Genom. 2021, 22, 261. https://doi.org/10.1186/s12864-021-07464-x.

  • 28.

    Zhao, T.; Ma, A.; Yang, S.; et al. Integrated Metabolome and Transcriptome Analyses Revealing the Effects of Thermal Stress on Lipid Metabolism in Juvenile Turbot Scophthalmus maximus. J. Therm. Biol. 2021, 99, 102937. https://doi.org/10.1016/j.jtherbio.2021.102937.

  • 29.

    Deng, K.; Yang, S.; Gu, D.; et al. Record-Breaking Heat Wave in Southern China and Delayed Onset of South China Sea Summer Monsoon Driven by the Pacific Subtropical High. Clim. Dyn. 2020, 54, 3751–3764. https://doi.org/10.1007/s00382-020-05203-8.

  • 30.

    Li, Y.; Ren, G.; Wang, Q.; et al. Changes in Marine Hot and Cold Extremes in the China Seas During 1982–2020. Weather Clim. Extrem. 2023, 39, 100553.

  • 31.

    Huang, J.; Fu, Z.; Liu, X.; et al. Splenic Tissue Injury and Physiological Response Mechanisms in Juvenile Yellowfin Tuna (Thunnus albacares) Under Acute Cold Stress. Dev. Comp. Immunol. 2025, 105421. https://doi.org/10.1016/j.dci.2025.105421.

  • 32.

    Amaral Carneiro, G.; Calì, M.; Cappelletti, E.; et al. Draft Genome Sequence of the Apple Pathogen Colletotrichum chrysophilum Strain M932. J. Plant Pathol. 2023, 105, 1141–1143. https://doi.org/10.1007/s42161-023-01353-w.

  • 33.

    Kim, D.; Paggi, J.M.; Park, C.; et al. Graph-Based Genome Alignment and Genotyping with HISAT2 and HISAT-Genotype. Nat. Biotechnol. 2019, 37, 907–915. https://doi.org/10.1038/s41587-019-0201-4.

  • 34.

    Xu, C.; Song, L.Y.; Li, J.; et al. MangroveDB: A Comprehensive Online Database for Mangroves Based on Multi-Omics Data. Plant Cell Environ. 2025, 48, 2950–2962. https://doi.org/10.1111/pce.15318.

  • 35.

    Lucchesi, S.; Montesi, G.; Polvere, J.; et al. Transcriptomic Analysis After SARS-CoV-2 mRNA Vaccination Reveals a Specific Gene Signature in Low-Responder Hemodialysis Patients. Front. Immunol. 2025, 16, 1508659.

  • 36.

    Varet, H.; Brillet-Guéguen, L.; Coppée, J.-Y.; et al. SARTools: A DESeq2-and EdgeR-Based R Pipeline for Comprehensive Differential Analysis of RNA-Seq Data. PLoS ONE 2016, 11, e0157022. https://doi.org/10.1371/journal.pone.0157022.

  • 37.

    Lancelle, L.J.; Potru, P.S.; Spittau, B.; et al. DgeaHeatmap: An R Package for Transcriptomic Analysis and Heatmap Generation. Bioinform. Adv. 2025, 5, vbaf194. https://doi.org/10.1093/bioadv/vbaf194.

  • 38.

    Nathaniel, T.P.; Chatterjee, N.S.; Varghese, T.; et al. Untargeted Metabolomics Reveals Membrane Lipid Remodeling and Dysregulation of Energy Metabolism in Genetically Improved Farmed Tilapia (Oreochromis niloticus) Under Acute Thermal Stress. Aquaculture 2025, 743094. https://doi.org/10.1016/j.aquaculture.2025.743094.

  • 39.

    Yang, X.; Wang, L.; Lu, K.; et al. High Temperature Changes the Structure and Function of Spotted Seabass (Lateolabrax maculatus) Tissues and Causes ER Stress and Mitochondrial Homeostasis Imbalance in Liver. Aquaculture 2025, 599, 742107.

  • 40.

    Sarapultsev, A.; Komelkova, M.; Lookin, O.; et al. Zebrafish as a Model Organism for Post-Traumatic Stress Disorder: Insights into Stress Mechanisms and Behavioral Assays. Biology 2025, 14, 939. https://doi.org/10.3390/biology14080939.

  • 41.

    Ahi, E.P.; Lindeza, A.S.; Miettinen, A.; et al. Transcriptional Responses to Changing Environments: Insights from Salmonids. Rev. Fish Biol. Fish. 2025. https://doi.org/10.1007/s11160-025-09928-9.

  • 42.

    Shi, X.; Cheng, Z.; Zheng, C.; et al. The Blood Transcriptome of Musk Deer Under Heat Stress Condition Reveals the Regulatory Mechanism of Genes to Maintain Homeostasis Metabolism. BMC Genom. 2025, 26, 400. https://doi.org/10.1186/s12864-025-11577-y.

  • 43.

    Dilawari, R.; Chaubey, G.K.; Priyadarshi, N.; et al. Antimicrobial Peptides: Structure, Function, Mechanism of Action and Therapeutic Applications in Human Diseases. Explor. Drug Sci. 2025, 3, 1008110. https://doi.org/10.37349/eds.2025.1008110.

  • 44.

    Chang, Q.; Zhang, Y.; Liu, X.; et al. Oxidative Stress in Antigen Processing and Presentation. MedComm. Oncol. 2025, 4, e70020. https://doi.org/10.1002/mog2.70020.

  • 45.

    Zhang, W.; Xu, X.; Li, J.; et al. Transcriptomic Analysis of the Liver and Brain in Grass Carp (Ctenopharyngodon idella) Under Heat Stress. Mar. Biotechnol. 2022, 24, 856–870. https://doi.org/10.1007/s10126-022-10148-6.

  • 46.

    Cecarini, V.; Gee, J.; Fioretti, E.; et al. Protein Oxidation and Cellular Homeostasis: Emphasis on Metabolism. Biochim. Et Biophys. Acta (BBA)-Mol. Cell Res. 2007, 1773, 93–104. https://doi.org/10.1016/j.bbamcr.2006.08.039.

  • 47.

    Malik, G.; Zhou, Y. Innate Immune Sensing of Influenza A Virus. Viruses 2020, 12, 755. https://doi.org/10.3390/v12070755.

  • 48.

    Le, J.; Kulatheepan, Y.; Jeyaseelan, S. Role of Toll-Like Receptors and Nod-Like Receptors in Acute Lung Infection. Front. Immunol. 2023, 14, 1249098. https://doi.org/10.3389/fimmu.2023.1249098.

  • 49.

    Tian, Y.; Li, L.; Long, H.; et al. Transcriptome Analyses Reveal the Molecular Response of Juvenile Greater Amberjack (Seriola dumerili) to Marine Heatwaves. Animals 2025, 15, 1871. https://doi.org/10.3390/ani15131871.

  • 50.

    Goutami, L.; Jena, S.R.; Moharana, A.K.; et al. HSPA2 Emerges as a Key Biomarker: Insights from Global Lysine Acetylproteomic Profiling in Idiopathic Male Infertility. Cell Stress Chaperones 2025, 30, 100090.

  • 51.

    Gariballa, N.; Ali, B.R. Endoplasmic Reticulum Associated Protein Degradation (ERAD) in the Pathology of Diseases Related to TGFβ Signaling Pathway: Future Therapeutic Perspectives. Front. Mol. Biosci. 2020, 7, 575608. https://doi.org/10.3389/fmolb.2020.575608.

  • 52.

    Pierre, A.S.; Gavriel, N.; Guilbard, M.; et al. Modulation of Protein Disulfide Isomerase Functions by Localization: The Example of the Anterior Gradient Family. Antioxid. Redox Signal. 2024, 41, 675–692. https://doi.org/10.1089/ars.2024.0561.

  • 53.

    Taylor, B.C.; Balko, J.M. Mechanisms of MHC-I Downregulation and Role in Immunotherapy Response. Front. Immunol. 2022, 13, 844866. https://doi.org/10.3389/fimmu.2022.844866.

  • 54.

    Thompson, M.R.; Kaminski, J.J.; Kurt-Jones, E.A.; et al. Pattern Recognition Receptors and the Innate Immune Response to Viral Infection. Viruses 2011, 3, 920.

  • 55.

    Brasseur, M.V.; Bakowski, C.; Christie, M.; et al. Heat Stress Responsive Genes Are Not Affected by Ocean Warming: Long-Term Environmental Monitoring and Acute Thermal Stress Experiments Identify Non-Overlapping Sets of Differentially Expressed Genes in a Marine Fish. Res. Sq. 2025. https://doi.org/10.21203/rs.3.rs-7212941/v1.

  • 56.

    Díaz-Villanueva, J.F.; Díaz-Molina, R.; García-González, V. Protein Folding and Mechanisms of Proteostasis. Int. J. Mol. Sci. 2015, 16, 17193–17230.

  • 57.

    Currie, J.; Manda, V.; Robinson, S.K.; et al. Simultaneous Proteome Localization and Turnover Analysis Reveals Spatiotemporal Features of Protein Homeostasis Disruptions. Nat. Commun. 2024, 15, 2207. https://doi.org/10.1038/s41467-024-46600-5.

  • 58.

    Rahman, N.S.A.; Zahari, S.; Syafruddin, S.E.; et al. Functions and Mechanisms of Protein Disulfide Isomerase Family in Cancer Emergence. Cell Biosci. 2022, 12, 129. https://doi.org/10.1186/s13578-022-00868-6.

  • 59.

    Schröder, M. Endoplasmic Reticulum Stress Responses. Cell. Mol. Life Sci. 2008, 65, 862–894. https://doi.org/10.1007/s00018-007-7383-5.

  • 60.

    Singh, M.K.; Shin, Y.; Ju, S.; et al. Heat Shock Response and Heat Shock Proteins: Current Understanding and Future Opportunities in Human Diseases. Int. J. Mol. Sci. 2024, 25, 4209. https://doi.org/10.3390/ijms25084209.

  • 61.

    Gao, C.; Peng, X.; Zhang, L.; et al. Proteome and Ubiquitylome Analyses of Maize Endoplasmic Reticulum under Heat Stress. Genes 2023, 14, 749. https://doi.org/10.3390/genes14030749.

  • 62.

    Xu, C.; Evensen, Ø.; Munang’andu, H.M. Transcriptome Analysis Shows that IFN-I Treatment and Concurrent SAV3 Infection Enriches MHC-I Antigen Processing and Presentation Pathways in Atlantic Salmon-Derived Macrophage/Dendritic Cells. Viruses 2019, 11, 464. https://doi.org/10.3390/v11050464.

  • 63.

    Esmaeili, N.; Martyniuk, C.J.; Kadri, S.; et al. Endoplasmic Reticulum Stress in Aquaculture Species. Rev. Aquac. 2025, 17, e70036. https://doi.org/10.1111/raq.70036.

Share this article:
How to Cite
Huang, J.; Fu, Z.; Bai, J.; Ma, Z. Transcriptomic Analysis of Liver Response in Juvenile Yellowfin Tuna (Thunnus albacares) Under Acute Heat Stress. Aquatic Life and Ecosystems 2026, 2 (1), 2. https://doi.org/10.53941/ale.2026.100002.
RIS
BibTex
Copyright & License
article copyright Image
Copyright (c) 2026 by the authors.