Germline DNA methylation in reef corals: patterns and potential roles in response to environmental change

Abstract

DNA methylation is an epigenetic mark that plays an inadequately understood role in gene regulation, particularly in non-model species. Because it can be influenced by the environment, DNA methylation may contribute to the ability of organisms to acclimatize and adapt to environmental change. We evaluated the distribution of gene body methylation in reef-building corals, a group of organisms facing significant environmental threats. Gene body methylation in six species of corals was inferred from in silico transcriptome analysis of CpG O/E, an estimate of germline DNA methylation that is highly correlated with patterns of methylation enrichment. Consistent with what has been documented in most other invertebrates, all corals exhibited bimodal distributions of germline methylation suggestive of distinct fractions of genes with high and low levels of methylation. The hypermethylated fractions were enriched with genes with housekeeping functions, while genes with inducible functions were highly represented in the hypomethylated fractions. High transcript abundance was associated with intermediate levels of methylation. In three of the coral species, we found that genes differentially expressed in response to thermal stress and ocean acidification exhibited significantly lower levels of methylation. These results support a link between gene body hypomethylation and transcriptional plasticity that may point to a role of DNA methylation in the response of corals to environmental change.

Epigenetics in natural animal populations

“…However, studies in turtles and alligators have also found different methylation patterns in other sex determination genes. For example, promoter methylation at SOX9 showed a converse methylation pattern Dimond & Roberts (2016) compared to cyp19a1 in alligator gonads (Parrott et al, 2014). These results suggest that DNA methylation could act as a key mediator integrating temperature into molecular mechanisms that determine sex in some animal species.…”

“…To study the epigenetic basic of phenotypic variation, it is useful for a system to exhibit a significant degree of phenotypic plasticity when responding to environmental changes (Dimond & Roberts, 2016). Good long-term data sets connecting environmental parameters with changes in phenotype and gene expression can also help to place functional work within a broader environmental context.…”

Rapid adaptive responses to climate change in corals

“…Furthermore, the low levels of correlation found between the transcriptome and the methylome of several multicellular organisms 32,33 , combined with the lack of a CpG methylation system in some of the most widely studied model animals, including the fruit fly Drosophila and the roundworm Caenorhabditis 34,35 , weakens the case for its significance as a universal regulator of gene expression 15,36 , and hence a universal mediator of TGP. In corals, DNA methylation levels correlate strongly with gene function; broadly and uniformly expressed 'housekeeping' genes are strongly methylated, whereas genes responsible for inducible or cell-specific functions are weakly methylated 37,38 (Fig. 2).…”

Ecological Epigenetics in Marine Metazoans

“…Studies on plants have dominated the literature on ecological epigenetics (Schrey et al, 2013;Baulcombe and Dean, 2014;Verhoeven et al, 2016), especially in response to stress (Wang et al, 2011;Grativol et al, 2012;Al-Lawati et al, 2016). On the marine side, epigenetic and epigenomic approaches are being used to explore areas such as (1) sources of phenotypic plasticity, as created by differential gene expression (Dixon et al, 2014;Dimond and Roberts, 2016;Marsh et al, 2016), (2) mechanisms involved in development (Riviere et al, 2013), and (3) a possible rapid response to anthropogenic environmental change (Putnam et al, 2016). These studies are mechanistic, but importantly also bridge to understanding adaptive capacity of marine organisms in response to environmental change (Calosi et al, 2016).…”