Ocean Acidification Induces Subtle Shifts in Gene Expression and DNA Methylation in Mantle Tissue of the Eastern Oyster (Crassostrea virginica)

Downey-Wall, Alan M.; Cameron, Louise P.; Ford, Brett M.; McNally, Elise M.; Venkataraman, Yaamini R.; Roberts, Steven B.; Ries, Justin B.; Lotterhos, Katie E.

doi:10.3389/fmars.2020.566419

Cited by 29 publications

(53 citation statements)

References 114 publications

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“…expression in Strongylocentrotus purpuratus and other invertebrates -Baseline patterns of genomic methylation, chromatin accessibility, transcription, and the relationships between these processes in S. purpuratus were consistent with those typically observed in other invertebrate lineages (Bonasio et al, 2012;Dixon et al, 2018;Downey-Wall et al, 2020;Flores et al, 2012;Gao et al, 2012;Gatzmann et al, 2018;Glastad et al, 2016;Kvist et al, 2018;Li-Byarlay et al, 2013;Libbrecht et al, 2016;Song et al, 2017;Zemach et al, 2010). Our results also further illuminate the relationship between baseline intragenic methylation and gene expression in metazoans; we observed an antagonistic relationship between intron and exon methylation in S. purpuratus such that a saturation of methylation in one genic feature reduced the additive effect of methylation on expression by the other.…”

Section: Relationships Between Dna Methylation Chromatin Accessibility and Genesupporting

confidence: 80%

“…GBM positively correlates with gene expression in cnidarians (Dixon, Liao, Bay, & Matz, 2018;Zemach et al, 2010), bivalve molluscs of Crassostrea sp. (Downey-Wall et al, 2020;Johnson, Sirovy, Casas, La Peyre, & Kelly, 2020), and arthropods (Bonasio et al, 2012;Gatzmann et al, 2018;Glastad, Gokhale, Liebig, & Goodisman, 2016;Kvist et al, 2018) with exceptions to this pattern evident in some species and cell types (de Mendoza et al, 2019;Flores et al, 2012;Wang, Song, et al, 2021). By contrast, inducible changes in invertebrate gene expression in response to environmental variation have frequently possessed insignificant relationships with differential GBM (Arsenault et al, 2018;Dixon et al, 2018;Downey-Wall et al, 2020;Strader et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…(Downey-Wall et al, 2020;Johnson, Sirovy, Casas, La Peyre, & Kelly, 2020), and arthropods (Bonasio et al, 2012;Gatzmann et al, 2018;Glastad, Gokhale, Liebig, & Goodisman, 2016;Kvist et al, 2018) with exceptions to this pattern evident in some species and cell types (de Mendoza et al, 2019;Flores et al, 2012;Wang, Song, et al, 2021). By contrast, inducible changes in invertebrate gene expression in response to environmental variation have frequently possessed insignificant relationships with differential GBM (Arsenault et al, 2018;Dixon et al, 2018;Downey-Wall et al, 2020;Strader et al, 2020). In some arthropods, molluscs, and nematodes, there is evidence that GBM aids in regulating alternative splicing and exon skipping (Flores et al, 2012;Gao et al, 2012;Li-Byarlay et al, 2013;Libbrecht, Oxley, Keller, & Kronauer, 2016;Song, Li, & Zhang, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Bogan

Strader

Hofmann

2021

Preprint

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Epigenetic processes are proposed to contribute to phenotypic plasticity. In invertebrates, DNA methylation commonly varies across environments and can correlate or causally associate with phenotype, but its role in transcriptional responses to the environment remains unclear. Maternal environments experienced by the sea urchin Strongylocentrotus purpuratus induce 3 - 6x greater differential CpG methylation in offspring larvae relative to larval developmental environments, suggesting a role for DNA methylation in transgenerational plasticity (TGP). However, a negligible association has been observed between differentially methylated and differentially expressed genes. What gene regulatory roles does invertebrate DNA methylation possess under environmental change, if any? We quantified DNA methylation and gene expression in S. purpuratus larvae exposed to different ecologically relevant conditions during gametogenesis (maternal conditioning) or embryogenesis (developmental conditioning). We modeled differential gene expression and differential splicing under maternal conditioning as functions of DNA methylation, incorporating variables for genomic feature and chromatin accessibility. We detected significant interactions between differential methylation, chromatin accessibility, and genic architecture associated with differential expression and splicing. Observed transcriptional responses to maternal conditioning were also 4 - 13x more likely when accounting for interactions between methylation and chromatin accessibility. Our results provide evidence that DNA methylation possesses multiple functional roles during TGP in S. purpuratus, but its effects are contingent upon other genomic and epigenomic states. Singularly unpredictive of transcription, DNA methylation is likely one cog in the epigenomic machinery contributing to environmental responses and phenotypic plasticity in S. purpuratus and other invertebrates.

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Section: Relationships Between Dna Methylation Chromatin Accessibility and Genesupporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Bogan

Strader

Hofmann

2021

Preprint

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“…Previous studies investigating oysters' calcification response to ocean acidification have either found no change in net calcification rates (Dickinson et al, 2012) or decreasing net calcification rates with increasing pCO 2 across a wide range of life stages (Beniash et al, 2010;Downey-Wall et al, 2020;Gazeau et al, 2007;Miller et al, 2009;Ries et al, 2009). Oyster larvae utilize the aragonite polymorph of CaCO 3 in shell development and are therefore considered more vulnerable to ocean acidification than juveniles or adults that utilize the less soluble calcite polymorph.…”

Section: Comparison With Prior Work Investigating Impact Of Ocean Acimentioning

confidence: 96%

“…This vulnerability may be exacerbated by the oyster's patchily distributed periostracum, which may confer less protection to their shell than the periostraca of other bivalves that possess more hydrophobic and continuous periostraca, such as clams and mussels (Ries et al, 2009). Eastern oysters also maintain their extrapallial fluid-their putative calcifying fluid-at lower pH than the surrounding seawater (Crenshaw, 1972;Crenshaw & Neff, 1969;Downey-Wall et al, 2020;Liu et al, 2020;Sutton et al, 2018), which may also increase their vulnerability to CO 2 -induced ocean acidification (Ries, 2011).…”

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confidence: 99%

Juvenile Eastern Oysters More Resilient to Extreme Ocean Acidification than Their Mud Crab Predators

Dodd

Grabowski

Piehler

et al. 2021

Geochem Geophys Geosyst

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Ocean acidification is predicted to impair marine calcifiers' abilities to produce shells and skeletons. We conducted laboratory experiments investigating the impacts of CO2‐induced ocean acidification (pCO2 = 478–519, 734–835, 8,980–9,567; Ωcalcite = 7.3–5.7, 5.6–4.3, 0.6–0.7) on calcification rates of two estuarine calcifiers involved in a classic predator‐prey model system: adult Panopeus herbstii (Atlantic mud crab) and juvenile Crassostrea virginica (eastern oyster). Both oyster and crab calcification rates significantly decreased at the highest pCO2 level. Notably, however, oysters maintained positive net calcification rates in the highest pCO2 treatment that was undersaturated with respect to calcite, while mud crabs exhibited net dissolution (i.e., net loss of shell mass) in calcite‐undersaturated conditions. Secondary electron imaging of oyster shells revealed minor microstructural alterations in the moderate‐pCO2 treatment, and major microstructural and macrostructural changes (including shell dissolution, delamination of periostracum) in the high‐pCO2 treatment. These results underscore the threat that ocean acidification poses for marine organisms that produce calcium carbonate shells, illustrate the strong biological control that some marine calcifiers exert over their shell‐building process, and shows that ocean acidification differentially impacts the crab and oyster species involved in this classical predator‐prey model system.

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Gene expression and epigenetic responses of the marine Cladoceran, Evadne nordmanni, and the copepod, Acartia clausi, to elevated CO₂

Aluru

Fields

Shema

et al. 2021

Ecology and Evolution

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The release of anthropogenic carbon emissions into the earth's atmosphere has resulted in changes in oceanic temperature and pH that have an impact on marine organisms and ecosystems (IPCC, 2021).IPCC scenarios project that pCO 2 will continue to climb resulting in an average sea surface temperature increase of 0.6°C-2.0°C and a pH drop of 0.06-0.32 units by the end of the century (IPCC, 2013).The rapid changes in these concurrent stressors is causing concern that some marine organisms may be unable to adapt and that this will reduce the resilience of marine ecosystems in which complex food webs maintain stability (Gledhill et al., 2015).

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Ocean Acidification Induces Subtle Shifts in Gene Expression and DNA Methylation in Mantle Tissue of the Eastern Oyster (Crassostrea virginica)

Cited by 29 publications

References 114 publications

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Juvenile Eastern Oysters More Resilient to Extreme Ocean Acidification than Their Mud Crab Predators

Gene expression and epigenetic responses of the marine Cladoceran, Evadne nordmanni, and the copepod, Acartia clausi, to elevated CO₂

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Ocean Acidification Induces Subtle Shifts in Gene Expression and DNA Methylation in Mantle Tissue of the Eastern Oyster (Crassostrea virginica)

Cited by 29 publications

References 114 publications

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Juvenile Eastern Oysters More Resilient to Extreme Ocean Acidification than Their Mud Crab Predators

Gene expression and epigenetic responses of the marine Cladoceran, Evadne nordmanni, and the copepod, Acartia clausi, to elevated CO2

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Product

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Gene expression and epigenetic responses of the marine Cladoceran, Evadne nordmanni, and the copepod, Acartia clausi, to elevated CO₂