Seasonal DNA Methylation Variation in the Flat Tree Oyster Isognomon Alatus from a Mangrove Ecosystem in North Biscayne Bay, Florida

Suárez-Ulloa, Victoria; Rivera-Casas, Ciro; Michel, Michelot

doi:10.2983/035.038.0108

Cited by 17 publications

(17 citation statements)

References 66 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Both spatial and temporal variation of abiotic factors have been shown to affect DNA methylation patterns in several mollusk species (Table 2). DNA methylation patterns can vary according to the seasonality (especially of temperature) in the oyster Isognomon alatus (Suarez-Ulloa et al, 2019) or according both to temperature and salinity in the Pacific abalone…”

Section: 3-dna Methylation Is Responsive To the Environment In Mollmentioning

confidence: 99%

Epigenetic inheritance and intergenerational effects in mollusks

Fallet

Luquet

David

et al. 2020

Gene

View full text Add to dashboard Cite

List of abbreviations 5mC5-methylcytosine, a cytosine that has been modified by the addition of a methyl group on its 5th carbon ADP Adenosine diphosphate AFLP Amplified fragment length polymorphism BLAST Basic Local Alignment Search Tool BS-Seq Bisulfite sequencing BS-PCR-Seq PCr amplification after bisulfite sequencing followed by sequencing Cd Cadium meDIP-seq Methylated DNA Immunoprecipitation sequencing MiRNAs Micro RNAs MSAP Methylation-sensitive amplified polymorphism MS-PCR Methylation-specific PCR pCO2 partial pressure of C02 PCR Polymerase chain reaction PTMs Post-Translational Modifications pH potential of Hydrogen qPCR quantitative Polymerase chain reaction RT-qPCR quantitative reverse transcription PCR RNA Ribonucleic acid RRBS Reduced representation bisulfite sequencing SAM S-adenosyl methionine SDS-PAGE Sodium Dodecil Sulfate PolyAcrylamide Gel Electrophoresis UV-HPLC Ultraviolet High performance liquid chromatography Abstract Recent insights in evolutionary biology have shed light on epigenetic variation that interacts with genetic variation to convey heritable information. An important characteristic of epigenetic changes is that they can be produced in response to environmental cues and passed on to later generations, potentially facilitating later genetic adaptation. While our understanding of epigenetic mechanisms in vertebrates is rapidly growing, our knowledge about invertebrates remains lower, or is restricted to model organisms. Mollusks in particular, are a large group of invertebrates, with several species important for ecosystem function, human economy and health. In this review, we attempt to summarize the literature on epigenetic and 4 intergenerational studies in mollusk species, with potential importance for adaptive evolution. Our review highlights that two molecular bearers of epigenetic information, DNA methylation and histone modifications, are key features for development in mollusk species, and both are sensitive to environmental conditions to which developing individuals are exposed. Further, although studies are still scarce, various environmental factors (e.g. predator cues, chemicals, parasites) can induce intergenerational effects on the phenotype (life-history traits, morphology, behaviour) of several mollusk taxa. More work is needed to better understand whether environmentally-induced changes in DNA methylation and histone modifications have phenotypic impacts, whether they can be inherited through generations and their role in intergenerational effects on phenotype. Such work may bring insight into the potential role of epigenetic in adaptation and evolution in mollusks.

show abstract

Section: 3-dna Methylation Is Responsive To the Environment In Mollmentioning

confidence: 99%

Epigenetic inheritance and intergenerational effects in mollusks

Fallet

Luquet

David

et al. 2020

Gene

View full text Add to dashboard Cite

show abstract

“…and thecosome pteropods, a clade of shelled pteropods considered to be a bellwether for the severity of global OA (Bednaršek et al, 2014a). Furthermore, epigenetic studies revealing the importance of DNA methylation for biological functions in molluscs (Gavery and Roberts, 2013;Riviere et al, 2013Riviere et al, , 2017Diaz-Freije et al, 2014;Lian et al, 2015;Garcia-Fernandez et al, 2017;Suarez-Ulloa et al, 2019) thus far have been heavily skewed toward bivalves and in particular, oysters, necessitating a broader assessment of diversity in environmental epigenetics across the speciose molluscan phylum.…”

Section: Introductionmentioning

confidence: 99%

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

2020

View full text Add to dashboard Cite

Epigenetic processes such as variation in DNA methylation may promote phenotypic plasticity and the rapid acclimatization of species to environmental change. The extent to which an organism can mount an epigenetic response to current and future climate extremes may influence its capacity to acclimatize or adapt to global change on ecological rather than evolutionary time scales. The thecosome pteropod Limacina helicina antarctica is an abundant macrozooplankton endemic to the Southern Ocean and is considered a bellwether of ocean acidification as it is highly sensitive to variation in carbonate chemistry. In this study, we quantified variation in DNA methylation and gene expression over time across different ocean acidification regimes. We exposed L. helicina antarctica to pCO 2 levels mimicking present-day norms in the coastal Southern Ocean of 255 µatm pCO 2 , present-day extremes of 530 µatm pCO 2 , and projected extremes of 918 µatm pCO 2 for up to 7 days before measuring global DNA methylation and sequencing transcriptomes in animals from each treatment across time. L. helicina antarctica significantly reduced DNA methylation by 29-56% after 1 day of exposure to 918 µatm pCO 2 before DNA methylation returned to control levels after 6 days. In addition, L. helicina antarctica exposed to 918 µatm pCO 2 exhibited drastically more differential expression compared to cultures replicating present-day pCO 2 extremes. Differentially expressed transcripts were predominantly downregulated. Furthermore, downregulated genes were enriched with signatures of gene body methylation. These findings support the potential role of DNA methylation in regulating transcriptomic responses by L. helicina antarctica to future ocean acidification and in situ variation in pCO 2 experienced seasonally or during vertical migration. More broadly, L. helicina antarctica was capable of mounting a substantial epigenetic response to ocean acidification despite little evidence of metabolic compensation or recovery of the cellular stress response in this species at future pCO 2 levels.

show abstract

“…In addition, seasonal changes in these parameters also drive subsequent variation in coral physiology (Scheufen et al, 2017). Contrary to the case of random environmental variation, the predictability of seasonal fluctuations can be conducive to the development and inheritance of plastic transcriptional profiles mediating phenotypic responses, regulated by epigenetic mechanisms [e.g., seasonal DNA methylation changes in bivalve mollusks (Suarez-Ulloa et al, 2019), plants (Ito et al, 2019) and birds (Viitaniemi et al, 2019)]. Indeed, seasonality produces dramatic physiological adjustments in corals, including changes in symbiont's abundance and pigmentation (Fitt et al, 2000;Thornhill et al, 2006), modifications of microbial community composition (Sharp et al, 2017), as well as the alteration of transcriptional profiles (Edge et al, 2008;Brady et al, 2011;Parkinson et al, 2018;Brener-Raffalli et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Therefore, understanding exposure-response relationships of these molecular mechanisms could potentially allow the quantification of the effects of the environment on phenotypic variation (Cortessis et al, 2012;Suarez-Ulloa et al, 2015;Etchegaray and Mostoslavsky, 2016), increasing our capacity to predict population responses after environmental change. While increasing evidence points to a relevant role of DNA methylation and other epigenetic mechanisms in plastic responses to environmental change in corals (Putnam et al, 2016;Dixon et al, 2018;Liew et al, 2018;Dimond and Roberts, 2020) and other marine organisms (Ryu et al, 2018;Eirin-Lopez and Putnam, 2019), there is limited understanding of the factors influencing dynamic epigenetic changes under nonstressed conditions, confounding the ability to determine the magnitude and extent of epigenetic responses under natural conditions (Suarez-Ulloa et al, 2019). In addition, solid baseline data of "natural response" to seasonal and diel cycles in most ecologically important organisms is lacking (Suarez-Ulloa et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…While increasing evidence points to a relevant role of DNA methylation and other epigenetic mechanisms in plastic responses to environmental change in corals (Putnam et al, 2016;Dixon et al, 2018;Liew et al, 2018;Dimond and Roberts, 2020) and other marine organisms (Ryu et al, 2018;Eirin-Lopez and Putnam, 2019), there is limited understanding of the factors influencing dynamic epigenetic changes under nonstressed conditions, confounding the ability to determine the magnitude and extent of epigenetic responses under natural conditions (Suarez-Ulloa et al, 2019). In addition, solid baseline data of "natural response" to seasonal and diel cycles in most ecologically important organisms is lacking (Suarez-Ulloa et al, 2019). This gap can be bridged by developing seasonal monitoring of coral epigenetic signatures, helping disentangle the molecular underpinnings of such epigenetic responses, their involvement in seasonal acclimatization, and their capacity to respond to factors driving global change in the Anthropocene.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

et al. 2020

View full text Add to dashboard Cite

Epigenetic modifications such as DNA methylation have been shown to participate in plastic responses to environmental change in a wide range of organisms, including scleractinian corals. Unfortunately, the current understanding of the links between environmental signals, epigenetic modifications, and the subsequent consequences for acclimatory phenotypic changes remain obscure. Such a knowledge gap extends also to the dynamic nature of epigenetic changes, hampering our ability to ascertain the magnitude and extent of these responses under natural conditions. The present work aims to shed light on these subjects by examining temporal changes in genomewide patterns of DNA methylation in the staghorn coral Acropora cervicornis in the island of Culebra, PR. During a 17-month period, a total of 162 polymorphic loci were identified using Methylation-Sensitive Amplified Polymorphism (MSAP). Among them, 83 of these restriction fragments displayed changes in DNA methylation that were significantly correlated to seasonal variation as determined mostly by changes in sea water temperature. Remarkably, the observed time-dependent variation in DNA methylation patterns is consistent across coral genets, coral source sites and sitespecific conditions studied. Overall, these results are consistent with a conserved epigenetic response to seasonal environmental variation. These findings highlight the importance of including seasonal variability into experimental designs investigating the role of epigenetic mechanisms such as DNA methylation in responses to stress.

show abstract

Seasonal DNA Methylation Variation in the Flat Tree Oyster Isognomon Alatus from a Mangrove Ecosystem in North Biscayne Bay, Florida

Cited by 17 publications

References 66 publications

Epigenetic inheritance and intergenerational effects in mollusks

Epigenetic inheritance and intergenerational effects in mollusks

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

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

Contact Info

Product

Resources

About