Effects of Florida Red Tides on histone variant expression and DNA methylation in the Eastern oyster Crassostrea virginica

Abstract

Massive algal proliferations known as Harmful Algal Blooms (HABs) represent one of the most important threats to coastal areas. Among them, the so-called Florida Red Tides (FRTs, caused by blooms of the dinoflagellate Karenia brevis and associated brevetoxins) are particularly detrimental in the southeastern U.S., causing high mortality rates and annual losses in excess of $40 million. The ability of marine organisms to cope with environmental stressors (including those produced during HABs) is influenced by genetic and epigenetic mechanisms, the latter resulting in phenotypic changes caused by heritable modifications in gene expression, without involving changes in the genetic (DNA) sequence. Yet, studies examining cause-effect relationships between environmental stressors, specific epigenetic mechanisms and subsequent responses are still lacking. The present work contributes to increase this knowledge by investigating the effects of Florida Red Tides on two types of mechanisms participating in the epigenetic memory of Eastern oysters: histone variants and DNA methylation. For that purpose, a HAB simulation was conducted in laboratory conditions, exposing oysters to increasing concentrations of K. brevis. The obtained results revealed, for the first time, the existence of H2A.X, H2A.Z and macroH2A genes in this organism, encoding histone variants potentially involved in the maintenance of genome integrity during responses to the genotoxic effect of brevetoxins. Additionally, an increase in H2A.X phosphorylation (γH2A.X, a marker of DNA damage) and a decrease in global DNA methylation were observed as the HAB simulation progressed. Overall, the present work provides a basis to better understand how epigenetic mechanisms participate in responses to environmental stress in marine invertebrates, opening new avenues to incorporate environmental epigenetics approaches into management and conservation programs.

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

“…The present work constitutes one of the few pioneering efforts investigating the role of epigenetic mechanisms during environmental responses in corals, more precisely to nutrient and thermal stress. In doing so, this work also expands recent efforts combining the study of multiple epigenetic mechanisms during environmental epigenetic responses in marine invertebrates, including histone variants (and their modifications) and DNA methylation (Gonzalez‐Romero et al, ; Li et al, ). The obtained results constitute the first description of the histone variant H2A.X and its phosphorylated form, gamma‐H2A.X, in a stony coral species.…”

“…However, the observed patterns were complex. First, basal gamma‐H2A.X levels (gamma‐H2A.X/H2A.X ratio >3) in corals are higher than those found in other eukaryotes including humans (Ji et al, ) and marine invertebrates (Gonzalez‐Romero et al, ). Such peculiarity can be interpreted in the context of the recurrent state of hyperoxia to which corals are subject during the day, resulting from the photosynthetic activity of symbiotic algae (Kuhl, Cohen, Dalsgaard, Jorgensen, & Revsbech, ; Shashar, Cohen, & Loya, ).…”

“…On one hand, increased H2A.X.1 and H2A.X.2 mRNA levels were found in Hydra exposed to the genotoxic agent bleomycin (Reddy et al, ). On the other, no expression changes were observed on variants H2A.X, H2A.Z, and macroH2A during the exposure of the Eastern oyster Crassostrea virginica to marine toxins (Gonzalez‐Romero et al, ). Nonetheless, both studies reported increased gamma‐H2A.X levels upon exposure to environmental stress (Gonzalez‐Romero et al, ; Reddy et al, ), supporting that the main functional role of this variant during DNA repair is regulated at a post‐translational level.…”

“…Epigenetic modifications in invertebrates can occur rapidly after exposure to environmental stress (Gonzalez‐Romero et al, ; Rivera‐Casas et al, ; Suarez‐Ulloa, Gonzalez‐Romero, & Eirin‐Lopez, ). Therefore, coral fragments were sampled at three different times during day 1 of exposure (1, 2, and 5 hr), day 2, day 7, and weekly thereafter for the next 4 weeks.…”

Examining the Role of DNA Methylation in Transcriptomic Plasticity of Early Stage Sea Urchins: Developmental and Maternal Effects in a Kelp Forest Herbivore

“…Environmental epigenetics has been examined in few marine invertebrate species (Marsh and Pasqualone, 2014;Ardura et al, 2017;Gavery and Roberts, 2017;Gonzalez-Romero et al, 2017;Li et al, 2017;Dixon et al, 2018;Liew et al, 2018;Baums et al, 2019;Hawes et al, 2019). While epigenetics can encompass a variety of non-genetic mechanisms such as histone modifications and small non-coding RNAs, the majority of marine environmental epigenetics research has focused on DNA methylation, in which cytosines, typically in a CpG dinucleotide context, contain a methyl group (Eirin-Lopez and Putnam, 2019).…”