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The epigenetic landscape of transgenerational acclimation to ocean warming

Nature Climate Change volume 8, pages 504–509 (2018)Cite this article

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Abstract

Epigenetic inheritance is a potential mechanism by which the environment in one generation can influence the performance of future generations1. Rapid climate change threatens the survival of many organisms; however, recent studies show that some species can adjust to climate-related stress when both parents and their offspring experience the same environmental change2,3. Whether such transgenerational acclimation could have an epigenetic basis is unknown. Here, by sequencing the liver genome, methylomes and transcriptomes of the coral reef fish, Acanthochromis polyacanthus, exposed to current day (+0 °C) or future ocean temperatures (+3 °C) for one generation, two generations and incrementally across generations, we identified 2,467 differentially methylated regions (DMRs) and 1,870 associated genes that respond to higher temperatures within and between generations. Of these genes, 193 were significantly correlated to the transgenerationally acclimating phenotypic trait, aerobic scope, with functions in insulin response, energy homeostasis, mitochondrial activity, oxygen consumption and angiogenesis. These genes may therefore play a key role in restoring performance across generations in fish exposed to increased temperatures associated with climate change. Our study is the first to demonstrate a possible association between DNA methylation and transgenerational acclimation to climate change in a vertebrate.

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Fig. 1: Experimental design and summary of the DMRs.
Fig. 2: Differential methylation patterns.
Fig. 3: Heatmaps of differentially methylated and net aerobic scope-correlated genes.
Fig. 4: DNA methylation patterns for thermal acclimation.

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Acknowledgements

This study was supported by the Competitive Research Funds OCRF-2014-CRG3-62140408 from the King Abdullah University of Science and Technology. This project was completed under JCU Ethics A1233 and A1415. T.Ryu acknowledges the support from the APEC Climate Center. P.L.M. was supported by the Australian Research Council (ARC) and P.L.M., H.D.V. and J.M.D. were supported by the ARC Centre of Excellence for Coral Reef Studies. We thank C. Ortiz Alvarez and E. J. Steinig (James Cook University) for assisting genomic DNA extraction for methylome sequencing. Figures were enhanced by I. Gromicho, scientific illustrator at King Abdullah University of Science and Technology (KAUST).

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Author notes

  1. These authors contributed equally: Taewoo Ryu and Heather D. Veilleux.

Authors and Affiliations

  1. APEC Climate Center, Busan, South Korea

    Taewoo Ryu

  2. KAUST Environmental Epigenetic Program, Division of Biological and Environmental Sciences & Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia

    Taewoo Ryu & Timothy Ravasi

  3. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia

    Heather D. Veilleux, Jennifer M. Donelson & Philip L. Munday

  4. School of Life Sciences, University of Technology Sydney, Broadway, New South Wales, Australia

    Jennifer M. Donelson

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Contributions

J.M.D. managed the fish rearing experiments and performed metabolism experiments. H.D.V. prepared samples for sequencing. H.D.V. extracted nucleic acids for genome and transcriptiome. T.Ryu extracted nucleic acids for methylome sequencing. T.Ryu, H.D.V. and J.M.D. selected samples for sequencing. T.Ryu designed and performed the computational analysis. T.Ryu and H.D.V. interpreted the results. T.Ryu, T.Ravasi, P.L.M., H.D.V. and J.M.D. wrote the manuscript. T.Ravasi and P.L.M. supervised the overall project.

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Correspondence to Philip L. Munday or Timothy Ravasi.

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Supplementary information

Supplementary Information

Supplementary Figures 1 & 2, Supplementary Tables 1–3, 5, 6, 8, 9

Supplementary Table 4

Genomic coordinates of identified differentially methylated regions (DMRs)

Supplementary Table 7

Differentially methylated and net aerobic scope (NAS)-correlated gene information

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Ryu, T., Veilleux, H.D., Donelson, J.M. et al. The epigenetic landscape of transgenerational acclimation to ocean warming. Nature Clim Change 8, 504–509 (2018). https://doi.org/10.1038/s41558-018-0159-0

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