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DNA Methylation Analysis Reveals Potential Mechanism in Takifugu rubripes Against Cryptocaryon irritans Infection

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Abstract

Takifugu rubripes (T. rubripes) is a valuable commercial fish, and Cryptocaryon irritans (C. irritans) has a significant impact on its aquaculture productivity. DNA methylation is one of the earliest discovered ways of gene epigenetic modification and also an important form of modification, as well as an essential type of alteration that regulates gene expression, including immune response. To further explore the anti-infection mechanism of T. rubripes in inhibiting this disease, we determined genome-wide DNA methylation profiles in the gill of T. rubripes using whole-genome bisulfite sequencing (WGBS) and combined with RNA sequence (RNA-seq). A total of 4659 differentially methylated genes (DMGs) in the gene body and 1546 DMGs in the promoter between the infection and control group were identified. And we identified 2501 differentially expressed genes (DEGs), including 1100 upregulated and 1401 downregulated genes. After enrichment analysis, we identified DMGs and DEGs of immune-related pathways including MAPK, Wnt, ErbB, and VEGF signaling pathways, as well as node genes prkcb, myca, tp53, and map2k2a. Based on the RNA-Seq results, we plotted a network graph to demonstrate the relationship between immune pathways and functional related genes, in addition to gene methylation and expression levels. At the same time, we predicted the CpG island and transcription factor of four immune-related key genes prkcb and mapped the gene structure. These unique discoveries could be helpful in the understanding of C. irritans pathogenesis, and the candidate genes screened may serve as optimum methylation-based biomarkers that can be utilized for the correct diagnosis and therapy T. rubripes in the development of the ability to resist C. irritans infection.

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The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

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Acknowledgements

We thank our colleagues who contributed to this study. We thank the Key Laboratory of Environment Controlled Aquaculture.

Funding

This work was supported by the National Natural Science Fund of China (No. 61942106094) and the Liaoning Province Doctor Startup Fund Program (No. 2021-BS-233).

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Authors and Affiliations

  1. School of Marine Sciences, Ningbo University, Ningbo, Zhejiang, 315211, People’s Republic of China

    Yu-qing Xia & Cheng-hua Li

  2. Key Laboratory of Environment Controlled Aquaculture (Dalian Ocean University), Ministry of Education, 52 Heishijiao Street, Dalian, 116023, People’s Republic of China

    Yu-qing Xia, Yi Yang, Yan-yun Liu, Jian-xin Cheng, Ying Liu & Peng-fei Liu

  3. College of Marine Technology and Environment, Dalian Ocean University, 52 Heishijiao Street, Dalian, 116023, People’s Republic of China

    Yi Yang, Yan-yun Liu & Peng-fei Liu

  4. College of Life Science, Liaoning Normal University, Dalian, 116081, People’s Republic of China

    Jian-xin Cheng

  5. College of Biosystems Engineering and Food Science, Zhejiang University, 866 Yuhangtang Road, Hangzhou, 310058, People’s Republic of China

    Ying Liu

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  1. Yu-qing Xia
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Contributions

Yu-qing Xia: performed the experiments, data curation, and writing, original draft. Yi-Yang: data curation. Yan-yun Liu and Jian-xin Cheng: analyzed the data. Ying Liu: contributed reagents/materials/analysis tools. Cheng-hua Li: investigation. Peng-fei Liu: reviewing.

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Xia, Yq., Yang, Y., Liu, Yy. et al. DNA Methylation Analysis Reveals Potential Mechanism in Takifugu rubripes Against Cryptocaryon irritans Infection. Mar Biotechnol 26, 288–305 (2024). https://doi.org/10.1007/s10126-024-10296-x

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