Skip to main content
SpringerLink
Log in

Whole-Genome Methylation Sequencing of Large Yellow Croaker (Larimichthys crocea) Liver Under Hypoxia and Acidification Stress

  • Research
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Large yellow croaker (Larimichthys crocea) is an important aquaculture species in China. This study analysed whole-genome methylation differences in liver tissues of young fish under different hypoxic and acidification conditions. Differentially methylated regions (DMRs) and differentially methylated genes (DMGs) were identified. Gene ontology (GO) and Kyoto encyclopaedia of genes and genomes (KEGG) enrichment analyses of DMGs were conducted to explore the mechanism of coping with hypoxic acidification. The main methylation type was CG, accounting for > 70% of total methylation, significantly higher than CHG and CHH methylation types. GO enrichment analysis of DMGs revealed strong enrichment of nervous system development, cell periphery, plasma membrane, cell junction organisation, cell junction, signalling receptor activity, molecular sensor activity, cell-linked tissue junction organisation, cell–cell adhesion and nervous system development. KEGG enrichment analysis of DMR-related genes identified cell adhesion molecules, cortisol synthesis and secretion and aldosterone synthesis and secretion as the three key pathways regulating the physiological responses to hypoxia and acidification. Long-term hypoxic and acidification stress affected the immune system, nervous system and stress responses of large yellow croaker. Whole-genome sequencing analysis of exposed tissues was used to investigate changes that occur in L. crocea in response to hypoxic and acidic conditions at the DNA methylation level. The findings contribute to our comprehensive understanding of functional methylation in large yellow croaker and will support future research on the response mechanisms of this species under different environmental pressures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The data used to support to the findings of this study are available from the corresponding author upon reasonable request.

References

  • Abdel-Tawwab M, Hagras AE, Elbaghdady HM, Monier MN (2014) Dissolved oxygen level and stocking density effects on growth, feed utilization, physiology, and innate immunity of Nile Tilapia, Oreochromis niloticus. J Applied Aquacult 26:340–355

    Article  Google Scholar 

  • Baker ME (2003) Evolution of glucocorticoid and mineralocorticoid responses: go fish. Endocrinology 144:4223–4225

    Article  CAS  PubMed  Google Scholar 

  • Beavo JA, Hardman JG, Sutherland EW (1971) Stimulation of adenosine 3′,5′-monophosphate hydrolysis by guanosine 3′,5′-monophosphate. J Biol Chem 246:3841–3846

    Article  CAS  PubMed  Google Scholar 

  • Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170

    Article  CAS  PubMed  Google Scholar 

  • Brauner C, Baker D (2009) Patterns of acid–base regulation during exposure to hypercarbia in fishes. Cardio-respiratory control in vertebrates. Springer. Berlin, Heidelberg, pp 43–63

    Google Scholar 

  • Bureau of Fishery, Ministry of Agriculture, People’s Republic of China (2022) Fisheries economic statistics. In China Fishery Yearbook; China Agricultural Press, Beijing, China, p 22

  • Bury N, Sturm A, Le RP, Lethimonier C, Ducouret B, Guiguen Y, Robinson-Rechavi M, Laudet V, Rafestin-Oblin M, Prunet P (2003) Evidence for two distinct functional glucocorticoid receptors in teleost fish. J Mol Endocrinol 31:141–156

    Article  CAS  PubMed  Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophysical Res Oceans 110:12

    Article  Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365–365

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Yuan G, Su J, Liu X (2019) Hematological analysis of Ctenopharyngodon idella, Megalobrama amblycephala and Pelteobagrus fulvidraco: morphology, ultrastructure, cytochemistry and quantification of peripheral blood cells. Fish Shellfish Immun 90:376–384

    Article  CAS  Google Scholar 

  • Chen L, Zhou J, Zhao Z, Zhu Y, Xing J, An J, Guo X (2023) Low expression of phosphodiesterase 2 (PDE2A) promotes the progression by regulating mitochondrial morphology and ATP content and predicts poor prognosis in hepatocellular carcinoma. Cells 12:68

    Article  CAS  Google Scholar 

  • Cheng W, Liu CH, Hsu JP, Chen JC (2002) Effect of hypoxia on the immune response of giant freshwater prawn Macrobrachium rosenbergii and its susceptibility to pathogen Enterococcus. Fish Shellfish Immun 13:351–365

    Article  Google Scholar 

  • Cooley SR, Doney SC (2009) Anticipating ocean acidification’s economic consequences for commercial fisheries. Environ Res Lett 4:024007

    Article  Google Scholar 

  • Doney SC, Ruckelshaus M, Emmett DJ, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37

    Article  Google Scholar 

  • Eby LA, Crowder LB (2004) Effects of hypoxic disturbances on an estuarine nekton assemblage across multiple scales. Estuaries 27:342–351

    Article  Google Scholar 

  • Eissa N, Wang HP (2016) Transcriptional stress responses to environmental and husbandry stressors in aquaculture species. Rev Aquacult 8:61–88

    Article  Google Scholar 

  • Everett MV, Antal CE, Crawford DL (2012) The effect of short-term hypoxic exposure on metabolic gene expression. J Exp Zool Part A 317:9–23

    Article  CAS  Google Scholar 

  • Fan X, Hou T, Sun T, Zhu L, Zhang S, Tang K, Wang Z (2019) Starvation stress affects the maternal development and larval fitness in zebrafish (Danio rerio). Sci Total Environ 695:133897

    Article  CAS  PubMed  Google Scholar 

  • Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goikoetxea A, Sadoul B, Blondeau BE, Aerts J, Blanc MO, Parrinello H, Barrachina C, Pratlong M, Geffroy B (2021) Genetic pathways underpinning hormonal stress responses in fish exposed to short-and long-term warm ocean temperatures. Ecol Indic 120:106937

    Article  Google Scholar 

  • Gray JS, Wu RSS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine environment. Mar Ecol Prog Ser 238:249–279

    Article  Google Scholar 

  • Greenwood AK, Butler PC, White RB, Demarco U, Pearce D, Fernald RD (2003) Multiple corticosteroid receptors in a teleost fish: distinct sequences, expression patterns, and transcriptional activities. Endocrinology 144:4226–4236

    Article  CAS  PubMed  Google Scholar 

  • Guh YJ, Tseng YC, Shao YT (2021) To cope with a changing aquatic soundscape: neuroendocrine and antioxidant responses to chronic noise stress in fish. Gen Comp Endocr 314:113918

    Article  CAS  PubMed  Google Scholar 

  • Huan PP, LÜ JJ, Sun DF, Gao BQ, Liu (2019) The cloning of the PtDNMT1 gene of Portunus trituberculatus and its expression analysis in low salinity adaptation. Prog Fishery Sci 40:92–100. (in Chinese with English abstract)

    Google Scholar 

  • Hynes RO, Lander AD (1992) Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68:303–322

    Article  CAS  PubMed  Google Scholar 

  • Ishimatsu A, Kikkawa T, Hayashi M, Lee KS, Kita J (2004) Effects of CO2 on marine fish: larvae and adults. J Oceanogr 60:731–741

    Article  CAS  Google Scholar 

  • Jonz MG, Nurse CA (2006) Ontogenesis of oxygen chemoreception in aquatic vertebrates. Respir Physiol Neurobiol 154:139–152

    Article  CAS  PubMed  Google Scholar 

  • Khan FU, Hu M, Kong H, Shang Y, Wang T, Wang X, Xu R, Lu W, Wang Y (2020) Ocean acidification, hypoxia and warming impair digestive parameters of marine mussels. Chemosphere 256:127096

    Article  CAS  PubMed  Google Scholar 

  • Kikkawa T, Ishimatsu A, Kita J (2003) Acute CO2 tolerance during the early developmental stages of four marine teleosts. Environ Toxicol 18:375–382

    Article  CAS  PubMed  Google Scholar 

  • Kong N, Zhao J, Zhao B, Liu J, Li F, Wang L, Song L (2023) Effects of high temperature stress on the intestinal histology and microbiota in Yesso scallop Patinopecten yessoensis. Mar Environ Res 105881

  • Le Guellec D, Morvan-Dubois G, Sire JY (2003) Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). Int J Dev Biol 48:217–231

    Article  Google Scholar 

  • Li M, Wang X, Qi C, Li E, Du Z, Qin JG, Chen L (2018) Metabolic response of Nile tilapia (Oreochromis niloticus) to acute and chronic hypoxia stress. Aquaculture 495:187–195

    Article  CAS  Google Scholar 

  • Li X, Li F, Zou G, Feng C, Sha H, Liu S, Liang H (2021) Physiological responses and molecular strategies in heart of silver carp (Hypophthalmichthys molitrix) under hypoxia and reoxygenation. Comp Biochem Phys D 40:100908

    CAS  Google Scholar 

  • Limoncella S, Lazzaretti C, Paradiso E, D’Alessandro S, Barbagallo F, Pacifico S, Guerrini R, Tagliavini S, Trenti T, Santi D (2022) Phosphodiesterase (PDE) 5 inhibitors sildenafil, tadalafil and vardenafil impact cAMP-specific PDE8 isoforms-linked second messengers and steroid production in a mouse Leydig tumor cell line. Mol Cell Endocrinol 542:111527

    Article  CAS  PubMed  Google Scholar 

  • Lugnier C (2006) Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109:366–398

    Article  CAS  PubMed  Google Scholar 

  • Mangi SC, Lee J, Pinnegar JK, Law RJ, Tyllianakis E, Birchenough SN (2018) The economic impacts of ocean acidification on shellfish fisheries and aquaculture in the United Kingdom. Environ Sci Policy 86:95–105

    Article  CAS  Google Scholar 

  • Melzner F, Gutowska M, Langenbuch M, Dupont S, Lucassen M, Thorndyke M, Bleich M, Pörtner HO (2009) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6:2313–2331

    Article  CAS  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9:211–268

    Article  Google Scholar 

  • Petruzzelli L, Takami M, Humes HD (1999) Structure and function of cell adhesion molecules. Am J Med 106:467–476

    Article  CAS  PubMed  Google Scholar 

  • Philip AM, Vijayan MM (2015) Stress-immune-growth interactions: cortisol modulates suppressors of cytokine signaling and JAK/STAT pathway in rainbow trout liver. PLoS ONE 10:e0129299

    Article  PubMed  PubMed Central  Google Scholar 

  • Pickering A, Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol Biochem 7:253–258

    Article  CAS  PubMed  Google Scholar 

  • Schreck CB (1993) Glucocorticoids: metabolism, growth, and development. The endocrinology of growth, development, and metabolism in vertebrates 367–392

  • Seliger B, Marincola FM, Ferrone S, Abken H (2008) The complex role of B7 molecules in tumor immunology. Trends Mol Med 14:550–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sollid J, De AP, Gundersen K, Nilsson GRE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673

    Article  PubMed  Google Scholar 

  • Sturm A, Bury N, Dengreville L, Fagart J, Flouriot G, Rafestin-Oblin M, Prunet P (2005) 11-deoxycorticosterone is a potent agonist of the rainbow trout (Oncorhynchus mykiss) mineralocorticoid receptor. Endocrinology 146:47–55

    Article  CAS  PubMed  Google Scholar 

  • Sui Y, Kong H, Huang X, Dupont S, Hu M, Storch D, Pörtner HO, Lu W, Wang Y (2016) Combined effects of short-term exposure to elevated CO2 and decreased O2 on the physiology and energy budget of the thick shell mussel Mytilus coruscus. Chemosphere 155:207–216

    Article  CAS  PubMed  Google Scholar 

  • Szyf M (2011) The implications of DNA methylation for toxicology: toward toxicomethylomics, the toxicology of DNA methylation. Toxicol Sci 120:235–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teles M, Soares A, Tort L, Guimarães L, Oliveira M (2017) Linking cortisol response with gene expression in fish exposed to gold nanoparticles. Sci Total Environ 584:1004–1011

    Article  PubMed  Google Scholar 

  • Tort L, Koumoundouros G (2010) Stress in farmed fish. Its consequences in health and performance. Rec Adv Aquac Res P55–83

  • Wang X, Feng Y, Zhang Z, Li C, Han H (2023) Balance dysfunction in large yellow croaker in response to ocean acidification. Sci Total Environ 162444

  • Wang X, Zhu H, Hu H, Ma G (2016) Effects of hypoxia on physiological status of Siberian sturgeon Acipenser baeri juveniles. Fisheries Sci 35:459–465

    Google Scholar 

  • Wang Y, Chen R, Wang Q, Yue Y, Gao Q, Wang C, Zheng H, Peng S (2022) Transcriptomic analysis of large yellow croaker (Larimichthys crocea) during early development under hypoxia and acidification stress. Vet Sci 9:632

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Jin S, Fu H, Qiao H, Sun S, Zhang W, Jiang S, Gong Y, Xiong Y, Wu Y (2019) Identification and characterization of the DMRT11E gene in the oriental river prawn Macrobrachium nipponense. Int J Mol Sci 20:1734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zhang HY, Fodjo EK, Kong C, Gu RR, Han F, Shen XS (2018) Temperature effect study on growth and survival of pathogenic Vibrio parahaemolyticus in Jinjiang oyster (Crassostrea rivularis) with rapid count method. J Food Quality 2018

  • Wen Z, Zou S, Chen M, Zhou H, Sun G, Feng Y (2021) DNA methylation level of genomic DNA of Apostichopus japonicus at different temperatures. Prog Fish Sci 42:46–54

    Google Scholar 

  • Wu R, Woo N (1984) Respiratory responses and tolerance to hypoxia in two marine teleosts, Epinephelus akaara (Temminck & Schlegel) and Mylio macrocephalus (Basilewsky). Hydrobiologia 119:209–217

    Article  Google Scholar 

  • Zhang X, Li Q, Yu H, Kong L (2017) Effects of air exposure on genomic DNA methylation in the Pacific oyster (Crassostrea gigas) J Fish Sci China 24:690–697 (in Chinese with English abstract)

  • Zhang X, Wang Y (2007) Studies on oxygen consumption rate and suffocation point of Pseudosciaena crocea Fry. J Economic Animal 11:148–152 (in Chinese with English abstract)

    Google Scholar 

  • Zupanc GK, Sîrbulescu RF (2012) Teleost fish as a model system to study successful regeneration of the central nervous system. New Perspect Regen 193–233

Download references

Acknowledgements

Not applicable.

Funding

This work was supported by grants from the National Key Research and Development Plan (grant number 2018YFD0900603) and the Central Nonprofit Basic Scientific Research Project for the Scientific Research Institutes of China (grant number 2020XT1001).

Author information

Author notes

  1. Yanfeng Yue and Yabing Wang contributed equally to this work and should be considered co-first authors.

Authors and Affiliations

  1. Key Laboratory of Marine and Estuarine Fisheries, Ministry of Agriculture, East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai, 200090, People’s Republic of China

    Yanfeng Yue, Yabing Wang, Bianbian Zhang, Jiao Zeng, Qian Wang, Cuihua Wang & Shiming Peng

Authors
  1. Yanfeng Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yabing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bianbian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiao Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cuihua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shiming Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived and designed the experiments: Yanfeng Yue, Yabing Wang, Shiming Peng. Performed the fish trial: Jiao Zeng, Yanfeng Yue, Yabing Wang. Collected and processed fish samples: Jiao Zeng, Yanfeng Yue, Yabing Wang. Performed the experiments and analyzed the data: Yanfeng Yue, Yabing Wang. Critically evaluated all the data and edited the manuscript: Yabing Wang, Qian Wang, Bianbian Zhang, Cuihua Wang, Shiming Peng. Writing – original draft: Yanfeng Yue, Yabing Wang. Writing – review & editing: Yabing Wang, Bianbian Zhang, Cuihua Wang, Shiming Peng. Project administration: Cuihua Wang, Shiming Peng, Yabing Wang. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Cuihua Wang or Shiming Peng.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 10 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yue, Y., Wang, Y., Zhang, B. et al. Whole-Genome Methylation Sequencing of Large Yellow Croaker (Larimichthys crocea) Liver Under Hypoxia and Acidification Stress. Mar Biotechnol 25, 567–579 (2023). https://doi.org/10.1007/s10126-023-10226-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-023-10226-3

Keywords

Search

Navigation