Coral epigenetic responses to nutrient stress: Histone H2A.X phosphorylation dynamics and DNA methylation in the staghorn coral Acropora cervicornis

Abstract

Nutrient pollution and thermal stress constitute two of the main drivers of global change in the coastal oceans. While different studies have addressed the physiological effects and ecological consequences of these stressors in corals, the role of acquired modifications in the coral epigenome during acclimatory and adaptive responses remains unknown. The present work aims to address that gap by monitoring two types of epigenetic mechanisms, namely histone modifications and DNA methylation, during a 7‐week‐long experiment in which staghorn coral fragments (Acropora cervicornis) were exposed to nutrient stress (nitrogen, nitrogen + phosphorus) in the presence of thermal stress. The major conclusion of this experiment can be summarized by two main results: First, coral holobiont responses to the combined effects of nutrient enrichment and thermal stress involve the post‐translational phosphorylation of the histone variant H2A.X (involved in responses to DNA damage), as well as nonsignificant modifications in DNA methylation trends. Second, the reduction in H2A.X phosphorylation (and the subsequent potential impairment of DNA repair mechanisms) observed after prolonged coral exposure to nitrogen enrichment and thermal stress is consistent with the symbiont‐driven phosphorus limitation previously observed in corals subject to nitrogen enrichment. The alteration of this epigenetic mechanism could help to explain the synergistic effects of nutrient imbalance and thermal stress on coral fitness (i.e., increased bleaching and mortality) while supporting the positive effect of phosphorus addition to improving coral resilience to thermal stress. Overall, this work provides new insights into the role of epigenetic mechanisms during coral responses to global change, discussing future research directions and the potential benefits for improving restoration, management and conservation of coral reef ecosystems worldwide.

Genome-Wide DNA Methylation Analysis Reveals a Conserved Epigenetic Response to Seasonal Environmental Variation in the Staghorn Coral Acropora cervicornis

“…Unfortunately, the DNA methylation trends characterized in the present work do not support this notion. While rapid epigenetic changes were observed by our own previous research in coral (Rodriguez-Casariego et al, 2018), the constant change in DNA methylation patterns observed in the present work is not consistent with a linear progression toward an acclimated state. Indeed, several loci follow a seasonal-like pattern returning to DNA methylation values similar to those measured during the same season in the previous year ( Figures 3G, 4).…”

“…Epigenetic landmarks, such as histone variants and DNA methylation, influence phenotypic plasticity in response to changes in environmental conditions and are, therefore, predictors of the general state of the organism in the face of environmental alterations and natural cycles (Rivière, 2014). Emerging evidence suggests that these mechanisms play an important role during responses to environmental changes, likely by regulating gene expression and maintaining DNA integrity throughout the entire lifespan of an organism (Roberts and Gavery, 2012;Dimond and Roberts, 2016;Liew et al, 2018;Rodriguez-Casariego et al, 2018). Recent studies on marine invertebrates [reviewed in Eirin-Lopez and Putnam (2019)] have shown that DNA methylation exerts a role on phenotypic acclimatization (Putnam et al, 2016;Liew et al, 2018;Durante et al, 2019) by modulating gene expression (Dixon et al, 2018).…”

Changes in Genome-Wide Methylation and Gene Expression in Response to Future pCO2 Extremes in the Antarctic Pteropod Limacina helicina antarctica

“…Overall, our results suggest that differential methylation of DNA and histones may jointly influence persistent transcriptomic responses by L. helicina antarctica to future pCO 2 extremes. Histone modifications (e.g., histone methylation) and subsequent changes in transcription have been shown to regulate development and responses to environmental stress in molluscs (Fellous et al, 2015(Fellous et al, , 2019Gonzalez-Romero et al, 2017) and other calcifying marine invertebrates (Rodriguez-Casariego et al, 2018). Interactions between chromatin structure and DNA methylation should be explored in greater functional detail in this system in order to substantiate these observations and understand their influence on pervasive and persistent downregulation by L. helicina antarctica under OA.…”

Gene Expression Patterns of Red Sea Urchins (Mesocentrotus Franciscanus) Exposed to Different Combinations of Temperature and pCO2 During Early Development

“…The dynamic changes in different epigenetic marks can act to regulate gene function without altering the DNA sequence, promoting phenotypic plasticity and potentially modulating the response to different environmental conditions [77][78][79]. Histone variants and modi cations may activate or repress transcription processes by altering chromatin structures, impacting the regions of the genome that are available for transcription [80], and have been shown to mediate responses to changing environmental conditions in marine organisms [81][82][83]. Here, histone binding and chromatin remodeling genes are positively correlated with the 17 °C gastrula treatment.…”