Patterns, dynamics, and potential roles of DNA methylation in reef corals and their allies
Dimond, James L
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Epigenetic processes, which contribute to gene regulation without affecting underlying DNA sequences, are increasingly recognized as molecular mechanisms that shape phenotypes. DNA methylation is the best understood epigenetic process and has been shown to mediate environmental effects on gene expression and phenotype in a wide range of taxa. However, most of what is known about DNA methylation is based on model organisms, particularly vertebrates, while much less is known about DNA methylation in other organisms such as invertebrates. Tropical reef corals are long-lived, sessile invertebrates that are thought to be particularly reliant on physiological acclimatization and phenotypic plasticity to cope with environmental variation. The underlying basis of this plasticity could lie, at least in part, in epigenetic mechanisms like DNA methylation. The aim of this dissertation research is to examine DNA methylation in corals with respect to its patterns, variability, response to change, and involvement in phenotypic and transcriptional plasticity. Chapter one explores patterns of evolutionary-scale DNA methylation in corals, using CpG depletion analysis to estimate methylation levels in publicly available transcriptome data from six coral species. 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. In three of the coral species, 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. Chapter two evaluates the hypothesis that DNA methylation patterns reflect phenotypic differences among Atlantic branching corals of the genus Porites. Using reduced representation genome sequencing, genetic and epigenetic diversity among 27 colonies of Porites spp. from Belize were compared. Contrary to expectations, epigenetic patterns were inconclusive, while genetic data showed clear separation of three distinct genetic groups. One of these groups exhibited significantly thicker branches, and branch thickness was a better predictor of genetic groups than depth, habitat or symbiont type. Relationships between genetic and epigenetic patterns suggest that epigenetic patterns reflect diverse environmental histories superimposed over a relatively small heritable component. Meanwhile, the clear genetic patterns revealed by high throughput sequencing suggest that this technique could hold promise for resolving the phylogeny of this taxonomically difficult group. Chapter three asks whether DNA methylation in corals exhibits plasticity in response to environmental change. Colonies of the mounding coral Porites astreoides on the Belize Barrier Reef were experimentally transplanted to a common garden in 2015 and resampled the following year. Methylation levels in both years were determined via reduced representation genome sequencing (RADseq). Methylation status was largely stable over time, with only ~2% change in methylation over the one-year period. However, there was evidence for convergence of the methylation state of corals after a year in a common environment together. The loci that changed their methylation status were associated with mRNAs and non-coding RNAs. This work suggests that while DNA methylation levels in corals are not fixed, their response to environmental change may be subtle. Chapter four is a functional genomics study testing the hypothesis that DNA methylation is associated with symbiotic state and alternative mRNA splicing, using symbiotic and aposymbiotic individuals of the sea anemone Anthopleura elegantissima. The study leveraged third-generation Oxford Nanopore sequencing for its full-length reads and ability to detect base modifications. A largely complete A. elegantissima draft genome was generated from aposymbiotic individuals. There was no strong evidence for significant modification of the methylome according to symbiotic state, however, three genomic regions with consistently different methylation according to symbiotic state were identified. The region exhibiting the strongest difference was associated with a DNA polymerase zeta that is noted for its role in translesion synthesis, which opens interesting questions about the biology of this symbiosis.
- Fisheries