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Intergenerational epigenetic inheritance in reef-building corals

Abstract

The perception that the inheritance of phenotypic traits operates solely through genetic means is slowly being eroded: epigenetic mechanisms have been shown to induce heritable changes in gene activity in plants1,2 and metazoans1,3. Inheritance of DNA methylation patterns provides a potential pathway for environmentally induced phenotypes to contribute to evolution of species and populations1,2,3,4,5. However, in basal metazoans, it is unknown whether inheritance of CpG methylation patterns occurs across the genome (as in plants) or as rare exceptions (as in mammals)4. Here, we show that DNA methylation patterns in a reef-building coral are determined by genotype and developmental stage, as well as by parental environment. Transmission of CpG methylation from adults to their sperm and larvae demonstrates genome-wide inheritance. Variation in the hypermethylation of genes in adults and their sperm from distinct environments suggests intergenerational acclimatization to local temperature and salinity. Furthermore, genotype-independent adjustments of methylation levels in stress-related genes were strongly correlated with offspring survival rates under heat stress. These findings support a role of DNA methylation in the intergenerational inheritance of traits in corals, which could extend to enhancing their capacity to adapt to climate change.

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Fig. 1: Data acquisition and summarized findings showing intergenerational inheritance of DNA methylation patterns in P. daedalea.
Fig. 2: Environmental origin changes in epigenotype are mostly independent of genotype in P. daedalea.
Fig. 3: DNA methylation profiles are associated with environmental origin in P. daedalea.
Fig. 4: DNA methylation profiles vary considerably across developmental stages in P. daedalea.

Data availability

Whole-genome bisulfite sequencing data can be found in NCBI BioProject PRJNA430328. Individual SRA accessions are listed in Supplementary Dataset 1c. Genomic sequences and annotations are available at http://pdae.reefgenomics.org/ (ref. 55).

Code availability

Scripts used to analyse methylation data (and the underlying theoretical justifications) are detailed at https://github.com/lyijin/working_with_dna_meth. Other analytical and plotting scripts, key intermediate files and further explanatory notes are available at https://doi.org/10.5281/zenodo.3558476 (v.1.0.0).

References

  1. 1.

    Jablonka, E. & Raz, G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84, 131–176 (2009).

    Google Scholar 

  2. 2.

    Lamke, J. & Baurle, I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 18, 124 (2017).

    Google Scholar 

  3. 3.

    Lim, J. P. & Brunet, A. Bridging the transgenerational gap with epigenetic memory. Trends Genet. 29, 176–186 (2013).

    CAS  Google Scholar 

  4. 4.

    Heard, E. & Martienssen, R. A. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157, 95–109 (2014).

    CAS  Google Scholar 

  5. 5.

    Eirin-Lopez, J. M. & Putnam, H. M. Marine environmental epigenetics. Annu. Rev. Mar. Sci. 11, 335–368 (2019).

    Google Scholar 

  6. 6.

    Moberg, F. & Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).

    Google Scholar 

  7. 7.

    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    CAS  Google Scholar 

  8. 8.

    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    CAS  Google Scholar 

  9. 9.

    van Oppen, M. J., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl Acad. Sci. USA 112, 2307–2313 (2015).

    Google Scholar 

  10. 10.

    Torda, G. et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7, 627–636 (2017).

    Google Scholar 

  11. 11.

    Liew, Y. J. et al. Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral. Sci. Adv. 4, eaar8028 (2018).

    Google Scholar 

  12. 12.

    Dixon, G., Liao, Y., Bay, L. K. & Matz, M. V. Role of gene body methylation in acclimatization and adaptation in a basal metazoan. Proc. Natl Acad. Sci. USA 115, 13342–13346 (2018).

    CAS  Google Scholar 

  13. 13.

    Li, Y. et al. DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia. Sci. Adv. 4, eaat2142 (2018).

    CAS  Google Scholar 

  14. 14.

    Howells, E. J. et al. Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob. Change Biol. 22, 2702–2714 (2016).

    Google Scholar 

  15. 15.

    Howells, E. J. et al. Species-specific trends in the reproductive output of corals across environmental gradients and bleaching histories. Mar. Pollut. Bull. 105, 532–539 (2016).

    CAS  Google Scholar 

  16. 16.

    Riegl, B. et al. Population collapse dynamics in Acropora downingi, an Arabian/Persian Gulf ecosystem-engineering coral, linked to rising temperature. Glob. Change Biol. 24, 2447–2462 (2018).

    Google Scholar 

  17. 17.

    Dixon, G. B., Bay, L. K. & Matz, M. V. Bimodal signatures of germline methylation are linked with gene expression plasticity in the coral Acropora millepora. BMC Genom. 15, 1109 (2014).

    Google Scholar 

  18. 18.

    Dimond, J. L. & Roberts, S. B. Germline DNA methylation in reef corals: patterns and potential roles in response to environmental change. Mol. Ecol. 25, 1895–1904 (2016).

    CAS  Google Scholar 

  19. 19.

    Wang, X. et al. Function and evolution of DNA methylation in Nasonia vitripennis. PLoS Genet. 9, e1003872 (2013).

    Google Scholar 

  20. 20.

    Lyko, F. et al. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol. 8, e1000506 (2010).

    Google Scholar 

  21. 21.

    Glastad, K. M., Gokhale, K., Liebig, J. & Goodisman, M. A. The caste- and sex-specific DNA methylome of the termite Zootermopsis nevadensis. Sci. Rep. 6, 37110 (2016).

    CAS  Google Scholar 

  22. 22.

    Rosic, N. N. & Dove, S. Mycosporine-like amino acids from coral dinoflagellates. Appl. Environ. Microbiol. 77, 8478–8486 (2011).

    CAS  Google Scholar 

  23. 23.

    Imbs, A. B. & Yakovleva, I. M. Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach. Coral Reefs 31, 41–53 (2012).

    Google Scholar 

  24. 24.

    Tolosa, I., Treignier, C., Grover, R. & Ferrier-Pages, C. Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis. Coral Reefs 30, 763–774 (2011).

    Google Scholar 

  25. 25.

    Hillyer, K. E., Tumanov, S., Villas-Boas, S. & Davy, S. K. Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian–dinoflagellate symbiosis. J. Exp. Biol. 219, 516–527 (2016).

    Google Scholar 

  26. 26.

    Ogawa, Y. & Imamoto, N. Nuclear transport adapts to varying heat stress in a multistep mechanism. J. Cell Biol. 217, 2341–2352 (2018).

    CAS  Google Scholar 

  27. 27.

    Kosako, H. et al. Phosphoproteomics reveals new ERK MAP kinase targets and links ERK to nucleoporin-mediated nuclear transport. Nat. Struct. Mol. Biol. 16, 1026–1035 (2009).

    CAS  Google Scholar 

  28. 28.

    Downs, C. A. et al. Cellular pathology and histopathology of hypo-salinity exposure on the coral Stylophora pistillata. Sci. Total Environ. 407, 4838–4851 (2009).

    CAS  Google Scholar 

  29. 29.

    Spector, A. A. Arachidonic acid cytochrome P450 epoxygenase pathway. J. Lipid Res. 50, S52–S56 (2009).

    Google Scholar 

  30. 30.

    Vin, H. et al. BRAF inhibitors suppress apoptosis through off-target inhibition of JNK signaling. eLife 2, e00969 (2013).

    Google Scholar 

  31. 31.

    Kim, E., Goraksha-Hicks, P., Li, L., Neufeld, T. P. & Guan, K. L. Regulation of TORC1 by Rag GTPases in nutrient response. Nat. Cell Biol. 10, 935–945 (2008).

    CAS  Google Scholar 

  32. 32.

    Grunewald, S., Paasch, U., Glander, H. J. & Anderegg, U. Mature human spermatozoa do not transcribe novel RNA. Andrologia 37, 69–71 (2005).

    CAS  Google Scholar 

  33. 33.

    Zimmer, R. K. & Riffell, J. A. Sperm chemotaxis, fluid shear, and the evolution of sexual reproduction. Proc. Natl Acad. Sci. USA 108, 13200–13205 (2011).

    CAS  Google Scholar 

  34. 34.

    Nakamura, N. Ubiquitination regulates the morphogenesis and function of sperm organelles. Cells 2, 732–750 (2013).

    Google Scholar 

  35. 35.

    Song, W. H., Yi, Y. J., Sutovsky, M., Meyers, S. & Sutovsky, P. Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization. Proc. Natl Acad. Sci. USA 113, E5261–E5270 (2016).

    CAS  Google Scholar 

  36. 36.

    Putnam, H. M., Davidson, J. M. & Gates, R. D. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol. Appl. 9, 1165–1178 (2016).

    CAS  Google Scholar 

  37. 37.

    Hughes, T. P. et al. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Change 9, 40–43 (2019).

    Google Scholar 

  38. 38.

    Middlebrook, R., Hoegh-Guldberg, O. & Leggat, W. The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J. Exp. Biol. 211, 1050–1056 (2008).

    Google Scholar 

  39. 39.

    Brown, B. E., Dunne, R. P., Edwards, A. J., Sweet, M. J. & Phongsuwan, N. Decadal environmental ‘memory’ in a reef coral? Mar. Biol. 162, 479–483 (2015).

    Google Scholar 

  40. 40.

    Bellantuono, A. J., Granados-Cifuentes, C., Miller, D. J., Hoegh-Guldberg, O. & Rodriguez-Lanetty, M. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS ONE 7, e50685 (2012).

    CAS  Google Scholar 

  41. 41.

    Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895–898 (2014).

    CAS  Google Scholar 

  42. 42.

    Hofmeister, B. T., Lee, K., Rohr, N. A., Hall, D. W. & Schmitz, R. J. Stable inheritance of DNA methylation allows creation of epigenotype maps and the study of epiallele inheritance patterns in the absence of genetic variation. Genome Biol. 18, 155 (2017).

    Google Scholar 

  43. 43.

    Lauss, K. et al. Parental DNA methylation states are associated with heterosis in epigenetic hybrids. Plant Physiol. 176, 1627–1645 (2018).

    CAS  Google Scholar 

  44. 44.

    van Oppen, M. J. H. et al. Shifting paradigms in restoration of the world’s coral reefs. Glob. Change Biol. 23, 3437–3448 (2017).

    Google Scholar 

  45. 45.

    Howells, E. J., Abrego, D., Vaughan, G. O. & Burt, J. A. Coral spawning in the Gulf of Oman and relationship to latitudinal variation in spawning season in the northwest Indian Ocean. Sci. Rep. 4, 7484 (2014).

    CAS  Google Scholar 

  46. 46.

    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12 (2011).

    Google Scholar 

  47. 47.

    Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571–1572 (2011).

    CAS  Google Scholar 

  48. 48.

    Liu, Y., Siegmund, K. D., Laird, P. W. & Berman, B. P. Bis-SNP: combined DNA methylation and SNP calling for Bisulfite-seq data. Genome Biol. 13, R61 (2012).

    CAS  Google Scholar 

  49. 49.

    Bhatia, G., Patterson, N., Sankararaman, S. & Price, A. L. Estimating and interpreting FST: the impact of rare variants. Genome Res. 23, 1514–1521 (2013).

    CAS  Google Scholar 

  50. 50.

    Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (Complete Samples). Biometrika 52, 591–611 (1965).

    Google Scholar 

  51. 51.

    Levene, H. in Contributions to Probability and Statistics Vol. 1 (ed. Olkin, I.) 278–292 (Stanford Univ. Press, 1960).

  52. 52.

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).

    Google Scholar 

  53. 53.

    Benjamini, Y. & Yekutieli, D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188 (2001).

    Google Scholar 

  54. 54.

    Alexa, A., Rahnenfuhrer, J. & Lengauer, T. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22, 1600–1607 (2006).

    CAS  Google Scholar 

  55. 55.

    Liew, Y. J., Aranda, M. & Voolstra, C. R. Reefgenomics.Org—a repository for marine genomics data. Database 2016, baw152 (2016).

    Google Scholar 

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Acknowledgements

We thank D. Abrego, G. Vaughan and D. McParland for assistance with fieldwork, coral spawning and the collection of environmental data. We thank the NYUAD Core Research Vessel and The Palms Dive Center for fieldwork support. We thank the Environment Agency Abu Dhabi and Fujairah Municipality for research permits and the KAUST Sequencing Core Facility for the sequencing of the libraries. The research reported in this publication was supported by the KAUST OSR under grant no. URF/1/3447-01-01, as well as baseline support to M.A.; and by NYUAD research grant no. AD105 to Y.I.

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Contributions

E.J.H, Y.I. and M.A. conceived and coordinated the project. M.A., X.W. and J.A.B provided resources. E.J.H. collected samples from the wild, performed controlled crosses and extracted DNA from fixed samples. C.T.M. constructed libraries for WGBS and RNA-seq. Y.J.L., Y.I. and M.A. analysed data. Y.J.L., E.J.H. and M.A. wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Manuel Aranda.

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The authors declare no competing interests.

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Peer review information Nature Climate Change thanks Eva Majerová and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Extended data

Extended Data Fig. 1 Methylation in P. daedalea is more commonly found in genic regions, and concentrated closer to the 5’ and 3’ ends.

(a) Genic regions are significantly more frequently methylated than intergenic regions (3.9% versus 3.0%; Fisher’s exact P < 10-300). (b) Methylation levels are bimodally distributed in exons, introns and intergenic regions. Exons have the highest methylation levels, followed by introns and intergenic regions. (c) Relative frequencies of methylated positions across a standardized gene model with flanking 4 kb regions indicate that methylated positions are more frequently found at both ends of the gene model. Solid lines depict transcriptional start site (left) and transcription termination site (right) while dotted lines delineate the borders of the indicated genomic feature. The widths of the features correspond to mean normalized lengths of the respective exons and introns in P. daedalea (exons, from left to right: 286 bp, 320 bp, 225 bp, 203 bp, 270 bp, 380 bp; introns, from left to right: 1,971 bp, 1,744 bp, 1,598 bp, 1,728 bp).

Extended Data Fig. 2 Per-origin principal components analysis of DNA methylation patterns in P. daedalea.

Plots show variation explained by the first three principal components of PCAs carried out separately on samples from Fujairah (top row) and Abu Dhabi samples (bottom row). Samples from adults (squares) and sperm (circles) tend to pair by colony identity. Samples from reciprocal larval crosses E7 x S8 and E8 x S7 (red triangles) are positioned midway between S7 and S8 along all plotted axes, suggesting equal contribution from both parents to their DNA methylation patterns. The sole egg sample, E8, is located close to S8 and A8, indicating that the transmission of epigenetic patterns from parent to either gamete type is unbiased.

Extended Data Fig. 3 Methylation trends against FST are origin-agnostic.

Genes were split into two groups, corresponding to genes with higher methylation in Abu Dhabi relative to Fujairah (red), and vice versa (blue). When correlated against genetic factors, both groups showed trends similar to Fig. 2, where methylation differences were calculated as absolute differences.

Extended Data Fig. 4 Outline of statistical tests performed.

Numbers denote biological replicates of different developmental stages and sample origins, while boxes denote the groupings used in the statistical tests. The initial GLM (green) tested whether both variables had significant interaction. Subsequently, the pair of t-tests (blue) identified genes that were differentially methylated across developmental stages, while the t-test (red) identified genes that were differentially methylated across sample origins.

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2.

Reporting Summary

Supplementary Dataset

Supplementary Data 1–8.

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Liew, Y.J., Howells, E.J., Wang, X. et al. Intergenerational epigenetic inheritance in reef-building corals. Nat. Clim. Chang. 10, 254–259 (2020). https://doi.org/10.1038/s41558-019-0687-2

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