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 {degrees}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.