Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral

Abstract

Over the last century, the anthropogenic production of CO2 has led to warmer (+0.74 °C) and more acidic (-0.1 pH) oceans1, resulting in increasingly frequent and severe mass bleaching events worldwide that precipitate global coral reef decline2,3. To mitigate this decline, proposals to augment the stress tolerance of corals through genetic and non-genetic means have been gaining traction4. Work on model systems has shown that environmentally induced alterations in DNA methylation can lead to phenotypic acclimatization5,6. While DNA methylation has been observed in corals7-10, its potential role in phenotypic plasticity has not yet been described. Here, we show that, similar to findings in mice11, DNA methylation significantly reduces spurious transcription in the Red Sea coral Stylophora pistillata, suggesting the evolutionary conservation of this essential mechanism in corals. Furthermore, we find that DNA methylation also reduces transcriptional noise by fine-tuning the expression of highly expressed genes. Analysis of DNA methylation patterns of corals subjected to long-term pH stress showed widespread changes in pathways regulating cell cycle and body size. Correspondingly, we found significant increases in cell and polyp sizes that resulted in more porous skeletons, supporting the maintenance of linear extension rates under conditions of reduced calcification. These findings suggest an epigenetic component in phenotypic acclimatization, providing corals with an additional mechanism to cope with climate change.

Sex‐specific changes in the aphid DNA methylation landscape

“…The same patterns were also observed using male methylation and gene expression data ( Figure S1). Taken together, these data suggest that DNA methylation in aphids may be involved in establishing and stabilising high gene expression, as has been suggested in corals (Liew et al, 2017) and holometabolous insects (Libbrecht et al, 2016;Patalano et al, 2015;Wang et al, 2013;Xiang et al, 2010).…”

Climate Change Impacts on Seagrass Meadows and Macroalgal Forests: An Integrative Perspective on Acclimation and Adaptation Potential

“…In the scleractinian coral Pocillopora damicornis, DNA methylation levels increased globally in response to increased pCO 2 levels (from ambient pH 7.9-7.65 to low pH 7.6-7.35) (Putnam et al, 2016). Accordingly, increasing DNA methylation likely contributed to phenotypic acclimation of the coral Stylophora pistillata under long-term exposure to reduced pH (Liew et al, 2017). These pioneering studies suggest that DNA methylation increases plasticity and adaptive potential in an ocean climate change context.…”

Convergence of DNA methylation profiles in a novel environment in the reef coral Porites astreoides

“…In a comparative study of two species of corals, Putnam et al (2016) found that global methylation levels of Montipora capitata did not change in response to reduced pH conditions, while those of Pocillopora damicornis were responsive. In another study of simulated ocean acidification conditions with Stylophora pistillata , Liew et al (2018b) observed modifications in methylation levels of genes involved in cell cycle and body size pathways that were reflected by phenotypic changes. Finally, in a reciprocal transplant study, Dixon et al (2018) reported genome-wide changes in methylation in Acropora millepora that were correlated with physiological and transcriptional plasticity.…”