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Molecular signatures of transgenerational response to ocean acidification in a species of reef fish

Nature Climate Change volume 6, pages 1014–1018 (2016)Cite this article

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Abstract

The impact of ocean acidification on marine ecosystems will depend on species capacity to adapt1,2. Recent studies show that the behaviour of reef fishes is impaired at projected CO2 levels3,4; however, individual variation exists that might promote adaptation. Here, we show a clear signature of parental sensitivity to high CO2 in the brain molecular phenotype of juvenile spiny damselfish, Acanthochromis polyacanthus, primarily driven by circadian rhythm genes. Offspring of CO2-tolerant and CO2-sensitive parents were reared at near-future CO2 (754 μatm) or present-day control levels (414 μatm). By integrating 33 brain transcriptomes and proteomes with a de novo assembled genome we investigate the molecular responses of the fish brain to increased CO2 and the expression of parental tolerance to high CO2 in the offspring molecular phenotype. Exposure to high CO2 resulted in differential regulation of 173 and 62 genes and 109 and 68 proteins in the tolerant and sensitive groups, respectively. Importantly, the majority of differences between offspring of tolerant and sensitive parents occurred in high CO2 conditions. This transgenerational molecular signature suggests that individual variation in CO2 sensitivity could facilitate adaptation of fish populations to ocean acidification.

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Figure 1: Sampling design of juvenile fish for molecular analysis of brain transcriptomes and proteomes.
Figure 2: Differential expression of transcripts and proteins for the four different comparisons of parental-sensitivity by CO2 rearing conditions.
Figure 3: Differential regulation of circadian rhythm genes for offspring of tolerant parents at high CO2 condition.

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Acknowledgements

This study was supported by the Australian Research Council (ARC) and the ARC Centre of Excellence for Coral Reef Studies (P.L.M.), the Office of Competitive Research Funds OCRF-2014-CRG3-62140408 from the King Abdullah University of Science and Technology (T.R., M.L.B., P.L.M., T.Ryu, C.S.), and the University of Oslo (G.E.N.). This project was completed under James Cook University (JCU) ethics permit A1828. We thank the Marine and Aquaculture Research Facilities Unit (JCU), Integrative Systems Biology Laboratory (KAUST), and Biosciences Core Laboratory (KAUST) for support and assistance.

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Authors and Affiliations

  1. Division of Biological and Environmental Sciences & Engineering and Division of Applied Mathematics and Computer Sciences, KAUST Environmental Epigenetic Program (KEEP), King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia

    Celia Schunter, Taewoo Ryu & Timothy Ravasi

  2. ARC Centre of Excellence for Coral Reef Studies and College of Marine and Environmental Sciences, James Cook University, Townsville, Queensland 4811, Australia

    Megan J. Welch

  3. APEC Climate Center, Busan 48058, South Korea

    Taewoo Ryu

  4. Proteomics and FACS facility, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia

    Huoming Zhang

  5. Division of Biological and Environmental Sciences & Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia

    Michael L. Berumen

  6. Department of Biosciences, University of Oslo, Section for Physiology and Cell Biology, Oslo NO-0316, Norway

    Göran E. Nilsson

  7. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia

    Philip L. Munday

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  1. Celia Schunter
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Contributions

M.J.W. and P.L.M. designed and managed the fish rearing experiments. M.J.W. performed the adult fish behavioural phenotyping. C.S. prepared the samples for RNA sequencing, and together with H.Z. protein samples for mass spectrometry. T.Ryu performed the genome assembly and gene annotation and wrote the corresponding part. C.S. analysed transcriptome expression data, and performed quantitative real-time PCR expression validation and variant analysis. C.S. analysed mass spectrometry data and integrated the data sets. G.E.N. assisted in interpreting the expression data. C.S., P.L.M., T.Ravasi and G.E.N. wrote the paper and all authors read and approved the final manuscript.

Corresponding authors

Correspondence to Philip L. Munday or Timothy Ravasi.

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The authors declare no competing financial interests.

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Schunter, C., Welch, M., Ryu, T. et al. Molecular signatures of transgenerational response to ocean acidification in a species of reef fish. Nature Clim Change 6, 1014–1018 (2016). https://doi.org/10.1038/nclimate3087

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