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

Rodríguez-Casariego, Javier; Mercado-Molina, Alex E.; García‐Souto, Daniel; Ortiz-Rivera, Ivanna M.; Lopes, Christian; Baums, Iliana B.; Sabat, Alberto M.; Eirín‐López, José M.

doi:10.3389/fmars.2020.560424

Cited by 33 publications

(26 citation statements)

References 106 publications

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“…We hypothesize preconditioning may enable pa-BI-1 to effectively regulate the expression of pa-GR through epigenetic modifications of the pa-GR regulatory elements. DNA methylation patterns vary between corals living in different environments and is dynamic over time in corals exposed to environmental changes, very likely enabling gene expression fine tuning in response to various conditions (65)(66)(67)(68).…”

Section: Discussionmentioning

confidence: 99%

Thermal preconditioning in a reef-building coral alleviates oxidative damage through a BI-1 mediated antioxidant response

Majerová

Drury

2021

Preprint

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Global coral reef decline is driven by the breakdown of the coral-algal symbiosis during temperature stress. Corals can acclimatize to higher temperatures on intra-generational timescales, but the complex cellular processes that underlie this ability and its trade-offs are poorly understood. We show that preconditioning-based improvements in thermal tolerance in Pocillopora acuta are accompanied by host increases in glutathione reductase (GR) activity and expression, which support a reducing intracellular environment that facilitates reactive oxygen scavenging and prevents DNA damage. We found a strong correlation between GR and BI-1 (Bax-inhibitor 1) expression in heat-stressed preconditioned corals and discovered an antioxidant response element (ARE) in the GR promoter, suggesting BI-1 could regulate GR expression in corals through the Nrf2/ARE pathway. To fortify this link, we developed an siRNA-mediated gene knockdown protocol and targeted the coral BI-1 gene. BI-1 knock-down decreased glutathione reductase expression, glutathione reductase activity and increased oxidative DNA damage in heat-stressed preconditioned corals, showing that enhanced regulation of antioxidant response during acute heat stress is a key mechanism that prevents oxidative DNA damage after preconditioning. These results describe the manipulation of an important molecular cascade at the core of symbiosis maintenance under thermal stress and show that induced symbiosis stability does not impact DNA integrity.

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Section: Discussionmentioning

confidence: 99%

Thermal preconditioning in a reef-building coral alleviates oxidative damage through a BI-1 mediated antioxidant response

Majerová

Drury

2021

Preprint

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“…To answer this question, we have integrated DNA methylation and RNA‐Seq analysis in this study, particularly focusing on the biomineralization tissue—mantle. This integration of ‘omics’ techniques such as transcriptomics and epigenomics is also identified as a promising method for understanding adaptive mechanisms of non‐model organisms to environmental factors and biomonitoring (Metzger & Schulte, 2016; Rodríguez‐Casariego et al, 2020; Suarez‐Ulloa et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Oyster biomineralization under ocean acidification: From genes to shell

Rajan

Yuan

et al. 2021

Global Change Biology

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Biomineralization is one of the key processes that is notably affected in marine calcifiers such as oysters under ocean acidification (OA). Understanding molecular changes in the biomineralization process under OA and its heritability, therefore, is key to developing conservation strategies for protecting ecologically and economically important oyster species. To do this, in this study, we have explicitly chosen the tissue involved in biomineralization (mantle) of an estuarine commercial oyster species, Crassostrea hongkongensis. The primary aim of this study is to understand the influence of DNA methylation over gene expression of mantle tissue under decreased ~pH 7.4, a proxy of OA, and to extrapolate if these molecular changes can be observed in the product of biomineralization—the shell. We grew early juvenile C. hongkongensis, under decreased ~pH 7.4 and control ~pH 8.0 over 4.5 months and studied OA‐induced DNA methylation and gene expression patterns along with shell properties such as microstructure, crystal orientation and hardness. The population of oysters used in this study was found to be moderately resilient to OA at the end of the experiment. The expression of key biomineralization‐related genes such as carbonic anhydrase and alkaline phosphatase remained unaffected; thus, the mechanical properties of the shell (shell growth rate, hardness and crystal orientation) were also maintained without any significant difference between control and OA conditions with signs of severe dissolution. In addition, this study makes three major conclusions: (1) higher expression of Ca2+ binding/signalling‐related genes in the mantle plays a key role in maintaining biomineralization under OA; (2) DNA methylation changes occur in response to OA; however, these methylation changes do not directly control gene expression; and (3) OA would be more of a ‘dissolution problem’ rather than a ‘biomineralization problem’ for resilient species that maintain calcification rate with normal shell growth and mechanical properties.

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“…Notably, acclimation capacity differs amongst coral species and appears inherently linked to the ability to mount rapid and lasting widespread transcriptomic changes [61][62][63][64] or reprogramming epigenetic marks [65][66][67] . In addition to acclimation within the lifetime of an animal, transgenerational plasticity might enable corals to acclimate to prevailing environmental conditions 48 .…”

Section: Adaptive Strategies Of Coral Hostsmentioning

confidence: 99%

Extending the natural adaptive capacity of coral holobionts

Voolstra

Suggett

Peixoto

et al. 2021

Nat Rev Earth Environ

142

131

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Tropical coral reefs cover only 0.1% of the seafloor yet provide habitat for >30% of all marine multicellular species 1 . Ecosystem services delivered through healthy tropical reefs are economically valued at around US $9,900,000 million per year 2 and sustain almost a billion people [3][4][5] . Despite their importance, catastrophic global loss of coral reefs owing to anthropogenic activity is fast becoming a reality 6 . For example, the 2015-2018 global coral bleaching event affected 74% of reefs worldwide, with >30% of coral cover lost on the Great Barrier Reef alone 7 . Additionally, coral cover in the Florida Reef Tract has declined by upwards of 90% over the last 50 years [8][9][10][11] .A global contributing factor to reef degradation is coral bleaching 12,13 . Without their microalgal symbionts (Fig. 1), corals lose their primary source of nutrition, leading to starvation, reduced fecundity, and reduced growth, often resulting in widespread coral mortality 14,15 . Trajectories for coral reefs under present CO 2 emission scenarios are dire, with 60% of all remaining coral reefs critically threatened, and 98% exposed to environmental conditions above the current thresholds considered necessary to maintain ecosystem function as soon as 2030 (reF. 16 ). The impact of ocean warming is exacerbated by the effects of ocean acidification 17 , deoxygenation 18 , and salinity changes 19 . Combined with local factors such as overfishing, coastal development, disturbance of the nutrient environment (water quality), and disease or predator outbreaks, the interrelated cumulative impacts all contribute to reduction in coral cover and declining reef ecosystem health [20][21][22][23][24][25][26][27] .Given the rate and extent at which climate change unfolds 28 , a widespread and shared concern is that the rate of environmental change could outpace the ability of coral holobionts to adapt to the changing environment 29 , concomitant with the increasing loss of coral reef cover 30 . Global mitigation of CO 2 emissions is unquestionably needed to stem the rate of declining reef health [30][31][32] . However, biological, ecological and socio-economic adaptations are critical partners to preserve reefs and delay the loss of coral populations until carbon mitigation is effectively implemented 30 . Reef protection through Marine Protected Areas and management practices reduces how local stressors compound global climate change impacts 27,31 . Nevertheless, the current state of reefs and their predicted further decline have sparked initiatives to prioritize reefs or corals that are less vulnerable to climate change and best positioned for regenerating other degraded reefs in the future [33][34][35] . Coral bleachingDiscolouration of coral tissue due to the loss of microalgal symbionts triggered by climate change-induced ocean warming and thermal stress anomalies.

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

Cited by 33 publications

References 106 publications

Thermal preconditioning in a reef-building coral alleviates oxidative damage through a BI-1 mediated antioxidant response

Thermal preconditioning in a reef-building coral alleviates oxidative damage through a BI-1 mediated antioxidant response

Oyster biomineralization under ocean acidification: From genes to shell

Extending the natural adaptive capacity of coral holobionts

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