Environmental epigenetics: A promising venue for developing next-generation pollution biomonitoring tools in marine invertebrates

Suárez-Ulloa, Victoria; González-Romero, Rodrigo; Eirín‐López, José M.

doi:10.1016/j.marpolbul.2015.06.020

Cited by 60 publications

(47 citation statements)

References 98 publications

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“…Under conditions of nutrient imbalance and/or thermal stress, such deleterious effects are likely to be exacerbated by the damage experienced by the photosynthetic machinery (Pogoreutz et al, ), as well as by the disruption of the symbiont's membrane composition (Wiedenmann et al, ). Given the well‐established role of histone H2A.X and its phosphorylated form during the activation of DNA repair mechanisms in eukaryotes (Maré Chal & Zou, ; Suarez‐Ulloa et al, ), the modifications observed in gamma‐H2A.X/H2A.X levels are consistent with the role of this mechanism mediating epigenetic effects during coral responses to nutrient stress, supporting the link between exposure to nutrient/thermal stress and the presence of DNA damage.…”

Section: Discussionsupporting

confidence: 63%

“…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.…”

Section: Methodsmentioning

confidence: 99%

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

Rodríguez-Casariego

Ladd

Shantz

et al. 2018

Ecology and Evolution

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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.

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Section: Discussionsupporting

confidence: 63%

Section: Methodsmentioning

confidence: 99%

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

Rodríguez-Casariego

Ladd

Shantz

et al. 2018

Ecology and Evolution

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“…Since epigenetic alterations can have a profound impact on gene expression, several studies have recognized the potential of metal-induced epigenetic alterations as informative factors in the risk assessment process, for instance as biomarkers of effect [22–24]. Furthermore, DNA methylation “footprints”caused by heavy metals could aid in introducing novel predictive tools for environmental quality monitoring [25].…”

Section: Introductionmentioning

confidence: 99%

Low levels of Cd induce persisting epigenetic modifications and acclimation mechanisms in the earthworm Lumbricus terrestris

2017

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Toxic effects of cadmium (Cd), a common soil pollutant, are still not very well understood, particularly in regard to its epigenetic impact. Therefore, the aim of this study was to assess DNA methylation changes and their persistence in the earthworm Lumbricus terrestris upon chronic low dose Cd exposure using methylation sensitive amplification polymorphism (MSAP). Moreover, the biomarker response and fitness of the earthworms, as well as the expression of detoxification-related genes (metallothionein (MT) and phytochelatin synthase (PCS)) was evaluated. Low levels of Cd caused an increase in genome-wide DNA methylation, which remained partly modified, even after several months of recovery in unpolluted soil. Increased cellular stress seemed to decrease after two weeks of exposure whereas fitness parameters remained unaffected by Cd, probably as a result from the activation of detoxification mechanisms like the expression of MTs. Interestingly, even though the level of Cd exposure was very low, MT expression levels indicate the development of acclimation mechanisms. Taken together, this study demonstrates that acclimation, as well as epigenetic modifications can occur already in moderately polluted environments. In addition, these effects can have long-lasting impacts on key species of soil invertebrates and might persist long after the actual heavy metal challenge has passed.

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“…In this regard, the presence of two potential estrogen receptor binding sites in the promoter of mussel H2A.Z.2 could account for the involvement of this histone in the response to endocrine disruptors in the marine environment (Goksoyr 2006). In addition, many of these environmental stressors (i.e., heavy metals and marine biotoxins) convey genotoxic effects requiring the activation DNA repair mechanisms in the cell (Suarez-Ulloa et al 2015). Since these mechanisms (and the implicit remodeling of chromatin) is also shared by germ cells during meiotic recombination, the participation of mussel H2A.Z.2 in these processes could account for its presence in both cell types (Rathke et al 2014).…”

Section: Phylogenetic Inferencementioning

confidence: 99%

“…Among these organisms, molluscs are remarkable candidates to study environmental responses and adaptation due to their ubiquitous distribution, easy accessibility and diverse lifestyles including sessile filter-feeding organisms (Gosling 2003). Indeed, bivalve molluscs constitute emerging models in epigenetics, as illustrated by recent studies examining the role of DNA methylation in the Pacific oyster (Gavery and Roberts 2010;Gavery and Roberts 2012;Suarez-Ulloa et al 2015). Nonetheless, the knowledge about other epigenetic mechanisms (most notably those involving structural chromatin components such as histone variants and their PTMs) and their role during environmental adaptive responses is still lacking (Santoro and Dulac 2015;Suarez-Ulloa et al 2015;Talbert and Henikoff 2014).…”

Section: Introductionmentioning

confidence: 99%

Characterization of mussel H2A.Z.2: a new H2A.Z variant preferentially expressed in germinal tissues fromMytilus

Rivera-Casas

González-Romero

Vizoso-Vazquez

et al. 2016

Biochem. Cell Biol.

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Histones are the fundamental constituents of the eukaryotic chromatin, facilitating the physical organization of DNA in chromosomes and participating in the regulation of its metabolism. The H2A family displays the largest number of variants among core histones, including the renowned H2A.X, macroH2A, H2A.B (Bbd), and H2A.Z. This latter variant is especially interesting because of its regulatory role and its differentiation into 2 functionally divergent variants (H2A.Z.1 and H2A.Z.2), further specializing the structure and function of vertebrate chromatin. In the present work we describe, for the first time, the presence of a second H2A.Z variant (H2A.Z.2) in the genome of a non-vertebrate animal, the mussel Mytilus. The molecular and evolutionary characterization of mussel H2A.Z.1 and H2A.Z.2 histones is consistent with their functional specialization, supported on sequence divergence at promoter and coding regions as well as on varying gene expression patterns. More precisely, the expression of H2A.Z.2 transcripts in gonadal tissue and its potential upregulation in response to genotoxic stress might be mirroring the specialization of this variant in DNA repair. Overall, the findings presented in this work complement recent reports describing the widespread presence of other histone variants across eukaryotes, supporting an ancestral origin and conserved role for histone variants in chromatin.

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Environmental epigenetics: A promising venue for developing next-generation pollution biomonitoring tools in marine invertebrates

Cited by 60 publications

References 98 publications

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

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

Low levels of Cd induce persisting epigenetic modifications and acclimation mechanisms in the earthworm Lumbricus terrestris

Characterization of mussel H2A.Z.2: a new H2A.Z variant preferentially expressed in germinal tissues fromMytilus

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