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Transcriptomic analysis of juvenile cobia in response to hypoxic stress

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Abstract

Cobia is an important cultured marine fish species in southern China. It is characterised by fast growth. Due to the effects of climate change on water oxygen levels and seawater temperatures, understanding the influence of environmental challenges on cobia culture has become very important. In this study, to explore the stress and adaptability of cobia (Rachycentron canadum) during hypoxia-reoxygenation conditions, the fish were exposed to an oxygen-deficient environment with dissolved oxygen (DO) level of 2.64 ± 0.25 mg/L. Liver tissue transcriptome sequencing was detected in the fish at acute hypoxia stress, after which fish were returned to normal DO levels (6.34 mg/L) for 8, 24, and 48 h. Comparative analysis of liver transcriptomes revealed that there were 1689, 651, 236, and 1150 differential genes in the hypoxia stress group (SC), reoxygenation-8h group (R8), reoxygenation-24h group (R24), and reoxygenation-48h group (R48), respectively. The differentially expressed genes were compared with the GO database. The main aggregated genes were related to gene ontology functional elements such as ribosome structural components, matrix-dependent cell migration, hormone activity, and oxidoreductase activity. The differentially expressed genes were compared with the Kyoto Encyclopedia of Genes and Genomes (KEGG) database, and a total of 43,054 differentially expressed genes were found to be enriched in 212 cases. For the first time, gene expression patterns in the liver of a juvenile’s cobia were examined in response to hypoxia. The results of this study contribute to further clarifying hypoxia’s effects on the liver of marine fish.

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References

  • Abdel-Tawwab M, Monier MN, Hoseinifar SH, Faggio C (2019) Fish response to hypoxia stress: growth, physiological, and immunological biomarkers. Fish Physiol Biochem 45(3):997–1013

    Article  CAS  PubMed  Google Scholar 

  • Amenyogbe E, Huang J-S, Chen G, Wang W-Z (2021) Probiotic potential of indigenous (Bacillus sp. RCS1, Pantoea agglomerans RCS2, and Bacillus cereus strain RCS3) isolated from cobia fish (Rachycentron canadum) and their antagonistic effects on the growth of pathogenic Vibrio alginolyticus, Vibrio harveyi, Streptococcus iniae, and Streptococcus agalactiae. Front Mar Sci 8:672213. https://doi.org/10.3389/fmars.2021.672213

    Article  Google Scholar 

  • Amenyogbe E, Yang E-J, Xie R-T, Huang J-S, Chen G (2022) Influences of indigenous isolates Pantoea agglomerans RCS2 on growth, proximate analysis, haematological parameters, digestive enzyme activities, serum biochemical parameters, antioxidants activities, intestinal morphology, disease resistance, and molecular immune response in juvenile’s cobia fish (Rachycentron canadum). Aquaculture 737942:0044–8486. https://doi.org/10.1016/j.aquaculture.2022.737942

    Article  CAS  Google Scholar 

  • Cai X-H, Huang Y-T, Zhang Z-P, Wang Y-L (2014) Hypoxia inducible factor-1 (HIF-1) and its research advance in aquatic animals. J Agri Biotechnol 22(1):119–132

    CAS  Google Scholar 

  • Cameron JS, Dewitt JP, Ngo TT, Yajnik T, Chan S, Chung E, Kang E (2013) Cardiac KATP channel alterations associated with acclimation to hypoxia in goldfish (Carassius auratus L.). Comp Biochem Physiol A Mol Integr Physiol. 164(4):554–64. https://doi.org/10.1016/j.cbpa.2012.12.020

    Article  CAS  PubMed  Google Scholar 

  • Casey TM (2002) Hypoxia causes downregulation of protein and RNA synthesis in noncontracting mammalian cardiomyocytes. Circ Res 90(7):777–783. https://doi.org/10.1161/01.res.0000015592.959

    Article  CAS  PubMed  Google Scholar 

  • Chee NT, Lohse I, Brothers SP (2019) mRNA-to-protein translation in hypoxia. Mol Cancer 18:49. https://doi.org/10.1186/s12943-019-0968-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen B.-X (2016) Identification and application of hypoxia-associated molecular markers in Megalobrama amblycephala[D]; Huazhong Agricultural University

  • Chi S, Tan B, Dong X, Yang Q, Liu H (2014) Effects of supplemental coated or crystallinemethionine in low-fishmeal diet on the growth performance and body composition of juvenile cobia Rachycentron canadum (Linnaeus). Chin J Oceanol Limnol 32:1297–1306

    Article  CAS  Google Scholar 

  • Chi S, Tan B, Dong X, Yang Q, Liu H, Xu Y, Huang H (2011) Effect of supplementation microcapsule or crystalline methionine in diets on related enzyme activity of cobia (Rachycentron canadum). J. Fish. Sci. China (Zhongguo Shuichan Kexue) 18

  • Cnaani A, McLean E (2009) Time-course response of cobia (Rachycentron canadum) to acute stress. Aquaculture 289(1–2):140–142. https://doi.org/10.1016/j.aquaculture.2008.12.016

    Article  CAS  Google Scholar 

  • Crear DP, Watkins BE, Friedrichs MAM, St-Laurent P, Weng KC (2020) Estimating shifts in phenology and habitat use of cobia in Chesapeake Bay under climate change. Front Mar Sci 7:579135. https://doi.org/10.3389/fmars.2020.579135

    Article  Google Scholar 

  • Detmar M, Brown LF, Berse B, Jackman RW, Elicker BM, Dvorak HF, Claffey KP (1997) Hypoxia regulates the expression of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) and its receptors in human skin. J Invest Dermatol 108(3):263–8. https://doi.org/10.1111/1523-1747.ep12286453

    Article  CAS  PubMed  Google Scholar 

  • Di Z-C, Zhou T, Xu Q-H (2018) Expression comparisons of heat shock proteins gene in gills of zebrafish exposed to both normoxia and hypoxia. J Dalian Ocean Univ 33(6):11–16

    Google Scholar 

  • Diaz RJ (2001) Overview of hypoxia around the world. J Environ Quality 30(2):275

    Article  CAS  Google Scholar 

  • Gong D, Xu L, Li W, Shang R, Chen J, Hu F, Wang S, Liua Q, Wu C, Zhou R, Zhang C, Tao M, Wang Y, Liu S (2020) Comparative analysis of liver transcriptomes associated with hypoxia tolerance in the gynogenetic blunt snout bream. Aquaculture, 735163https://doi.org/10.1016/j.aquaculture.2020.735163

  • Guo H-Y, Cheng G-H, Li Y-J, Zhang H, Qin K-L (2016) The high throughput sequencing technology and its application in biology. Contemporary Animal Husbandry 12:61–65

    Google Scholar 

  • Guo X (2005). Hemoglobin mechanism of hypoxia toleration in Tibetan chick embryo [D]; China Agricultural University

  • Heath AG (1988) Anaerobic and aerobic energy metabolism in brain and liver tissue from rainbow trout (Salmo gairdneri) and bullhead catfish (Ictalurus nebulosus). J Exp Zool 248(2):140–146

    Article  CAS  Google Scholar 

  • Huang C-Y, Lin H-C, Lin C-H (2015) Effects of hypoxia on ionic regulation, glycogen utilisation and antioxidative ability in the gills and liver of the aquatic air-breathing fish Trichogastermicrolepis. Comparative Biochem Physiol Part A: Mole Integr Physiol 179:25–34

    Article  CAS  Google Scholar 

  • Huang J-S, Guo Z-X, Zhang J-D, Wang W-Z, Wang Z-L, Amenyogbe E, Chen G (2021) Effects of hypoxia-reoxygenation conditions on serum chemistry indicators and gill and liver tissues of cobia (Rachycentroncanadum). Aquaculture Rep 20:2352–5134. https://doi.org/10.1016/j.aqrep.2021.100692

    Article  Google Scholar 

  • Huang JS, Zhi L, Chen G, Zhang J, Guo Z, Hong Y (2019) Acute hypoxia stress on blood biochemical indexes of large-sized juvenile cobia (Rachycentron canadum). Haiyang Xuebao 41(6):76–84

    Google Scholar 

  • Kang J, Ma X, He S (2017) Evidence of high-altitude adaptation in the glyptosternoid fish, Creteuchiloglanis macropterus from the Nujiang River obtained through transcriptome analysis. BMC Evol Biol 17:229. https://doi.org/10.1186/s12862-017-1074-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai KP, Li J-W, Tse AC-K, Chan T-F, Wu RS-S (2016) Hypoxia alters steroidogenesis in female marine medaka through miRNAs regulation. Aquatic Toxicol 172:1–8. https://doi.org/10.1016/j.aquatox.2015.12.012

    Article  CAS  Google Scholar 

  • Lando D (2002) Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 295(5556):858–861

    Article  CAS  PubMed  Google Scholar 

  • Lang KJD, Kappel A, Goodall GJ (2002) Hypoxia-inducible factor-1α mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. 13(5): 1792-1801

  • Li HL, Lin HR, Xia JH (2017) Differential gene expression profiles and alternative isoform regulations in gill of Nile tilapia in response to acute hypoxia. Marine Biotechnol 19(6):551–562

    Article  CAS  Google Scholar 

  • Li FG, Chen J, Jiang XY, Zou SM (2015) Transcriptome analysis of blunt snout bream (Megalobrama amblycephala) reveals putative differential expression genes related to growth and hypoxia. PLoS One 10:e0142801

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J-G, Wang S-Y, Wu X-N (2014) Whole transcriptome sequencing technology and its application in leukemia and lymphoma research. Int J Gene 37(3):124–128

    CAS  Google Scholar 

  • Li W, Tan H, Liu J, Hu J, Cui J, Wang S, Liu Q, Hu F, Ren L, Tao M, Zhao R, Yang C, Qin Q, Liu S (2019) Comparative analysis of testis transcriptomes associated with male infertility in triploid cyprinid fish. Reprod Fertil Dev 31:248–260

    Article  CAS  PubMed  Google Scholar 

  • Li X-L, Shi H-M, Xia H-Y, Zhou Y-P, Qiu Y-W (2014) Seasonal hypoxia and its potential forming mechanisms in the Mirs Bay, the northern South China Sea. Continental Shelf Res 80:1–7. https://doi.org/10.1016/j.csr.2014.03.003

    Article  Google Scholar 

  • Liao X, Lei C, Peng X, Guoqing L, Michael W, Xiaowen S, Songlin C, Marc R-R (2013) Transcriptome analysis of crucian carp (Carassius auratus), an important aquaculture and hypoxia-tolerant species. PLoS One 8:e62308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J-W, Mai K-S, Xu W, Zhang Y-J, Zhou H-H, Ai Q-H (2016) Effects of dietary glutamine on activities of nonspecific immune related enzymes and HIF-1α expression after hypoxia of half-smooth tongue sole post larvae. Acta Hydrobiologica Sinica 40(4):736–743

    Google Scholar 

  • Liu Y, Li E, Xu C, Su Y, Qin JG, Chen L, Wang X (2018) Brain transcriptome profiling analysis of Nile tilapia (Oreochromis niloticus) under long-term hypersaline stress. Frontiers in Physiology, 9https://doi.org/10.3389/fphys.2018.00219

  • Luo Y (2013) Nutrition requirement of dietary protein and optimal replacement of fish meal protein by rapeseed meal and corn gluten meal in cobia, Rachycentron canadum L. Ocean University of China, China ((MA. Sc. dissertation), in Chinese with English abstract)

  • Mandic M, Todgham AE, Richards JG (2009) Mechanisms and evolution of hypoxia tolerance in fish. Proceed Royal Soc B: Biol Sci 276(1657):735–744

    Article  CAS  Google Scholar 

  • Martinez LM (2006) Effects of long-term hypoxia on enzymes of carbohydrate metabolism in the Gulf killifish. Fundulus grandis J Exp Biol 209(19):3851–3861

    Article  CAS  PubMed  Google Scholar 

  • Mohindra V, Tripathi RK, Singh RK (2013) Molecular characterisation and expression analysis of PPP1R3C in hypoxia-tolerant Indian catfish, Clarias batrachus (Linnaeus, 1758) under hypoxia. Gene 530(1):127–133

    Article  CAS  PubMed  Google Scholar 

  • Mu Y, Li W, Wei Z, He L, Zhang W, Chen X (2020) Transcriptome analysis reveals molecular strategies in gills and heart of large yellow croaker (Larimichthys crocea) under hypoxia stress. Fish & Shellfish Immunol. https://doi.org/10.1016/j.fsi.2020.06.028

    Article  Google Scholar 

  • Nicholas SA, Sumbayev VV (2010) The role of redox-dependent mechanisms in the downregulation of ligand-induced Toll-like receptors 7, 8 and 4-mediated HIF-1α prolyl hydroxylation. Immunol Cell Biol 88(2):180–186

    Article  CAS  PubMed  Google Scholar 

  • Olsvik PA, Vibeke V, Lie KK, Hevrøy EM (2013) Transcriptional responses to temperature and low oxygen stress in Atlantic salmon studied with next-generation sequencing technology. BMC Genomics 14:817–837

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan Y, Chen D-X, Song X-H, Zhang X, Li L-Y (2017) Transcriptome characterisation for Scrophularia ningpoensis based on high-throughput sequencing technology and related genes for synthesis of terpenoid compounds. China J Chinese Materia Medica 42(13):2460–2466

    Google Scholar 

  • Qi D, Chao Y, Wu R, Xia M, Chen Q, Zheng Z (2018) Transcriptome analysis provides insights into the adaptive responses to hypoxia of a schizothoracine fish (Gymnocypris eckloni). Front Physiol 9. https://doi.org/10.3389/fphys.2018.01326

  • Qi Y-X, Liu Y-B, Rong W-H (2011) RNA-Seq and its applications: a new technology for transcriptomics. Hereditas 33(11):1191–1202

    CAS  PubMed  Google Scholar 

  • Qu W-D, Zhao H-Q (2009) Research progress on the role of HIF-1 in promoting angiogenesis under hypoxic conditions. J Oral Sci Res 25(2):234–236

    CAS  Google Scholar 

  • Rankin EB, Rha J, Selak MA, Unger TL, Keith B, Liu Q, Haase VH (2009) Hypoxia-inducible factor 2 regulates hepatic lipid metabolism. Mol Cell Biol 29:4527–4538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rojas DA, Perez-Munizaga DA, Centanin,L, Antonelli M, Wappner P, Allende ML, Reyes AE (2007). Cloning of hif-1alpha and hif-2alpha and mRNA expression pattern during development in zebrafish. 7(3): 339-345. https://doi.org/10.1016/j.modgep.2006.08.002

  • Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nature Rev Mole Cell Biol 5(5):343–354

    Article  CAS  Google Scholar 

  • Shang EH, Wu RS (2004) Aquatic hypoxia is a teratogen and affects fish embryonic development. Environ Sci Technol 38:4763–4767. https://doi.org/10.1021/es0496423

    Article  CAS  PubMed  Google Scholar 

  • Smith RW, Houlihan DF, Nilsson GN, Alexandre J (1996) Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol-Regulatory, Integr Comparative Physiol 271(4):897–904

    Article  Google Scholar 

  • Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E (1998) Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mole Cell Biol 18(6):3112–3119. https://doi.org/10.1128/MCB.18.6.3112

    Article  CAS  Google Scholar 

  • Storz JF, Scott GR, Cheviron ZA (2010) Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. J Exp Biol 213(Pt 24):4125–4136. https://doi.org/10.1242/jeb.048181

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun L, Liu S, Bao L, Li Y, Feng J, Liu Z (2015) Claudin multigene family in channel catfish and their expression profiles in response to bacterial infection and hypoxia as revealed by meta-analysis of RNA-Seq datasets. Comp Biochem Physiol Part D Genomics Proteomics 13:60–69

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Li X-B, Fang J (2013) Hypoxia and tumors. Chinese Bullet Life Sci 25(2):206–217

    Google Scholar 

  • Sun H-C (2006) The influence of HIF-1α and microvessel density as well as apoptosis associated index on the prognosis of pancreatic adenocarcinoma [D]; Zhe Jiang University

  • Sun S, Xuan F, Fu H, Zhu J, Ge X, Gu Z (2015) Transciptomic and histological analysis of hepatopancreas, muscle and gill tissues of oriental river prawn (Macrobrachium nipponense) in response to chronic hypoxia. BMC Genomics 16:491

    Article  PubMed  PubMed Central  Google Scholar 

  • Ton C, Stamatiou D, Liew C-C (2003) Gene expression profile of zebrafish exposed to hypoxia during development. Physiol Genomics 13(2):97–106

    Article  CAS  PubMed  Google Scholar 

  • Trasvi A-Arenas CH, Garcia-Triana A, Peregrino-Uriarte AB, Yepiz-Plascencia G (2013) White shrimp Litopenaeusvannamei catalase: gene structure, expression and activity under hypoxia and reoxygenation. Comp Biochem Physiol Part B: Biochem Mole Biol 164(1):44–52

    Article  Google Scholar 

  • Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci USA 105:15452–15457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C-Y, Guo M-Z, Liu X-Y, Liu Y (2015) Structural variation detection algorithm in high-throughput sequencing data. Intelligent Comput App 5(1):1–4

    Google Scholar 

  • Wang RN, Yoshida K, Toki T, Sawada T, Uechi T, Okuno Y, Sato-Otsubo A, Kudo K, Kamimaki I, Kanezaki R, Shiraishi Y, Chiba K, Tanaka H, Terui K, Sato T, Iribe Y, Ohga S, Kuramitsu M, Hamaguchi I, Ohara A, Hara J, Goi K, Matsubara K, Koike K, Ishiguro A, Okamoto Y, Watanabe K, Kanno H, Kojima S, Miyano S, Kenmochi N, Ogawa S, Ito E (2015) Loss of function mutations in RPL27 and RPS27 identified by whole-exome sequencing in Diamond-Blackfan anaemia. Br J Haematol 168(6):854–64. https://doi.org/10.1111/bjh.13229

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Yang L, Wu B, Song Z, He S (2015) Transcriptome analysis of the plateau fish (Triplophysa dalaica): implications for adaptation to hypoxia in fishes. Gene 565:211–220

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zhang S-Y (2017) Recent studies on the evolution of mammalian flight using high-throughput sequencing technology. Chinese Sci Bullet 62(7):631–634

    Article  Google Scholar 

  • Xiao W, Yang S, Zhu Z, Feng S, Li K (2007) Characterisation of the full-length cDNA, chromosomal localization, and polymorphism of the porcine RPLP0 gene. J Genet Genomics. 34(2):104–108. https://doi.org/10.1016/S1673-8527(07)60011-3

    Article  Google Scholar 

  • Xu K, Wen M, Duan W, Ren L, Hu F, Xiao J, Wang J, Tao M, Zhang C, Wang J, Zhou Y, Zhang Y, Liu Y, Liu S (2015) Comparative analysis of testis transcriptomes from triploid and fertile diploid cyprinid fish. Biol Reprod 92:95

    Article  PubMed  Google Scholar 

  • Xu S, Ying T, Li S (2011) Advance on PPAR-γ function. J Northeast Agri Univ 42(9):1–6

    Google Scholar 

  • Yasuda S, Sato T, Maekawa S, Aoyama S, Fukao Y, Yamaguchi J (2014) Phosphorylation of Arabidopsis ubiquitin ligase ATL31 is critical for plant carbon/nitrogen nutrient balance response and controls the stability of 14-3-3 proteins. J Biol Chem 289(22):15179–15193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11(2):R14. https://doi.org/10.1186/gb-2010-11-2-r14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu M-C (2017) Molecular adaption of the schizothoracine fishes in the phased uplifting of Qinghai-Tibetan Plateau revealed by transcriptome comparisons. Shanghai Ocean University

  • Zhang G, Zhao C, Wang Q, Gu Y, Li Z, Tao P, Chen J, Yin S (2017) Identification of HIF-1 signaling pathway in Pelteobagrus vachelli using RNA-Seq: effects of acute hypoxia and reoxygenation on oxygen sensors, respiratory metabolism, and hematology indices. J Comp Physiol B 187(7):931–943. https://doi.org/10.1007/s00360-017-1083-8

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Lin C, Fu F, Zhong X, Peng B, Yan H, Zhang J, Zhang W, Wang P, Ding X, Zhang W, Zhao L (2017) Comparative transcriptome analysis of flower heterosis in two soybean F1 hybrids by RNA-seq. PLoS One 12:e0181061

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Chen H, Zhou Q, Zhu F (2016) Effects of glutamine on antioxidant capacity and nonspecific immunity of juvenile yellow catfish (Pelteoobagrusfulvidraco). Chinese J Animal Nutrition 28(3):759–765

    CAS  Google Scholar 

  • Zhang Q-Y (2000) The structure and function of PPAR and its biological role. J Environ Hygiene 27(5):284–288

    Google Scholar 

  • Zhang W-J, Qing G-L (2013) Glutamine metabolism and cancer. Chinese Bullet Life Sci 11:73–78

    Google Scholar 

  • Zhong XP, Wang D, Zhang YB, Gui JF (2009) Identification and characterisation of hypoxia-induced genes in Carassius auratus blastulae embryonic cells using suppression subtractive hybridisation. Comp Biochem Physiol B Biochem Mol Biol 152:161–170. https://doi.org/10.1016/j.cbpb.2008.10.013

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q-C, Wu Z-H, Tan B-P, Chi S-Y, Yang Q-H (2006) Optimal dietary methionine requirement for juvenile cobia (Rachycentron canadum). Aquaculture 258:551–557

    Article  CAS  Google Scholar 

  • Zhu L, Lu Y-L, Feng L-S, Zhang S-X (2019) Effects of hypoxia exercise induced miR-27/PPARγ on fatty acids metabolism in gastrocnemius of obese rat. China Sport Sci 39(6):55–61

    Google Scholar 

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Funding

This work was supported by grants from Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang) (ZJW-2019-06) and the China Agriculture Research System of MOF and MARA (CARS-47).

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Authors and Affiliations

  1. Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang), Fisheries College of Guangdong Ocean University, Zhanjiang, China

    Jian-Sheng Huang, Zhi-Xiong Guo, Jian-Dong Zhang, Wei-Zheng Wang, Zhong-Liang Wang, Eric Amenyogbe & Gang Chen

  2. Guangdong Provincial Key Laboratory of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang, China

    Jian-Sheng Huang, Jian-Dong Zhang & Gang Chen

  3. Guangdong Evergreen Feed Industry Co., Ltd, Zhanjiang, China

    Rui-Tao Xie

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Contributions

Jian-Sheng Huang participated in the data curation, project administration, data analysis, and original article writing. Zhi-Xiong Guo participated in the data collection, Jian-Dong Zhang participated in the data collection, Wei-Zheng Wang participated in the data collection, Zhong-Liang Wang supervised the project, and Rui-Tao Xie supervised the project. Eric Amenyogbe did the writing, review, and edited the original article. Gang Chen planned and designed the experiments and acquired funding.

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Correspondence to Eric Amenyogbe or Gang Chen.

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This study was conducted in accordance with the guidelines of Guangdong Ocean University Research Council for the care and use of laboratory animals (approval number: GDOU-LAE-2020-013).

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Huang, JS., Guo, ZX., Zhang, JD. et al. Transcriptomic analysis of juvenile cobia in response to hypoxic stress. Aquacult Int 31, 931–955 (2023). https://doi.org/10.1007/s10499-022-01007-1

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