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

Abstract

Phenotypic acclimatization is an organismal response to environmental change that may be rooted in epigenetic mechanisms. In reef building corals, organisms that are severely threatened by environmental change, some evidence suggests that DNA methylation is an environmentally responsive mediator of acclimatization. We investigated changes in DNA methylation of the reef coral Porites astreoides in response to simulated environmental change.Coral colonies were sampled from a variety of habitats on the Belize Barrier Reef and transplanted to a common garden for one year. We used restriction site associated DNA sequencing, including a methylation-sensitive variant, to subsample the genome and assess changes in DNA methylation levels after a year in the common garden. Methylation changes among the 629 CpG loci we recovered were subtle, yet coral methylomes were more similar to each other after a year in the common garden together, indicating convergence of methylation profiles in the common environment. Differentially methylated loci showed matches with both coding and non-coding RNA sequences with putative roles in intracellular signaling, apoptosis, gene regulation, and epigenetic crosstalk. There was a weak but positive and significant relationship between genetic and epigenetic variation, providing evidence of methylation 1 heritability. Altogether, our results suggest that DNA methylation in P. astreoides is at least somewhat responsive to environmental change, reflective of the environment, and heritable, characteristics necessary for methylation to be implicated as part of potential transgenerational acclimatization responses.

Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa

“…cavernosa were methylated and primarily located in intergenic regions (>60% for all CpGs and methylated CpGs). This is comparable with the DNA methylation levels observed in other marine invertebrates (Gavery & Roberts, 2013; Strader et al, 2020; Venkataraman et al, 2020), including the relatively stress resistant corals Porites astreoides (Dimond & Roberts, 2020) and Montipora capitata (Trigg et al, 2021). Remarkably, methylation levels are significantly higher than those reported for the cnidarian model Aiptasia sp.…”

“…Epigenetic regulation is ubiquitous in all eukaryotes, based on the fundamental role that epigenetic mechanisms play in genome packing and functional organization within the cell nucleus. In corals, several studies have already reported evidence of epigenetic responses to different types of environmental stressors such as thermal stress, ocean acidification, and eutrophication, among others (Putnam et al, 2016; Liew et al, 2018; Dimond et al, 2017; Putnam et al, 2016; Liew et al, 2018; Rodriguez‐Casariego et al, 2018), as well as to broad environmental change (Rodríguez‐Casariego et al, 2020; Dimond & Roberts, 2020; Durante et al, 2019; Liew et al, 2020), with links to transcriptional plasticity (Dixon et al, 2018; Li et al, 2018). Since the symbiotic partners of corals also constitute part of (and therefore shape) their environment, the present work hypothesizes that transitions in these populations will require phenotypic acclimatory responses in the coral host, facilitated by epigenetic modifications.…”

Epigenetic and genetic population structure is coupled in a marine invertebrate

“…However, by further comparing genome-wide summary statistics and PCAs at the individual level, we revealed the significant relationship between interindividual patterns in methylation and genetic variation, with 27% of variation in inter-individual methylation differences explained by genetic distance. Similar analyses have found significant correlations in reef-building coral (Dimond & Roberts 2020) and humans (Carja et al 2017). By only focusing on measures of population differentiation, previous marine invertebrate studies may have missed couplings between methylation and genetic patterns.…”

Invertebrate methylomes provide insight into mechanisms of environmental tolerance and reveal methodological biases

“…Whereas this does not necessarily indicate a bias in our methods, it highlights the need to account for the biological characteristics of a species when designing an experiment and evaluating results. Also when comparing across species, given genetic–epigenetic correlations, particularly in the case of DNA methylation and the requirement for a CpG sequence target site (Dimond & Roberts, 2020; Johnson et al, 2020), variation in genome architecture, gene number and content will impact the presence and use of DNA methylation as a mechanism of gene expression regulation.…”