Differential DNA methylation in Pacific oyster reproductive tissue in response to ocean acidification

Abstract

Background There is a need to investigate mechanisms of phenotypic plasticity in marine invertebrates as negative effects of climate change, like ocean acidification, are experienced by coastal ecosystems. Environmentally-induced changes to the methylome may regulate gene expression, but methylome responses can be species- and tissue-specific. Tissue-specificity has implications for gonad tissue, as gonad-specific methylation patterns may be inherited by offspring. We used the Pacific oyster (Crassostrea gigas) — a model for understanding pH impacts on bivalve molecular physiology due to its genomic resources and importance in global aquaculture— to assess how low pH could impact the gonad methylome. Oysters were exposed to either low pH (7.31 ± 0.02) or ambient pH (7.82 ± 0.02) conditions for 7 weeks. Whole genome bisulfite sequencing was used to identify methylated regions in female oyster gonad samples. C- > T single nucleotide polymorphisms were identified and removed to ensure accurate methylation characterization. Results Analysis of gonad methylomes revealed a total of 1284 differentially methylated loci (DML) found primarily in genes, with several genes containing multiple DML. Gene ontologies for genes containing DML were involved in development and stress response, suggesting methylation may promote gonad growth homeostasis in low pH conditions. Additionally, several of these genes were associated with cytoskeletal structure regulation, metabolism, and protein ubiquitination — commonly-observed responses to ocean acidification. Comparison of these DML with other Crassostrea spp. exposed to ocean acidification demonstrates that similar pathways, but not identical genes, are impacted by methylation. Conclusions Our work suggests DNA methylation may have a regulatory role in gonad and larval development, which would shape adult and offspring responses to low pH stress. Combined with existing molluscan methylome research, our work further supports the need for tissue- and species-specific studies to understand the potential regulatory role of DNA methylation.

Genome-wide DNA methylation and transcription analysis reveal the potential epigenetic mechanism of heat stress response in the sea cucumber Apostichopus japonicus

“…Previous studies have also shown that DNA methylation in the body wall and intestinal tissues of A. japonicus mainly occurred at the CpG sites during Vibrio splendens infestation, aestivation, and heat stress (Sun et al, 2020;Yang et al, 2020;Wen et al, 2021). In addition, the DNA methylation pattern in A. japonicus was consistent with research results on the Pacific abalone, Yesso scallop, Pacific oyster (Huang et al, 2021;Yuan et al, 2021;Venkataraman et al, 2022), and other metazoans (Lechner et al, 2013). Although CpG was the main type of DNA methylation, there were some differences in the characteristics of CpG in different regions of the genome.…”

Ocean acidification does not overlook sex: Review of understudied effects and implications of low pH on marine invertebrate sexual reproduction

“…If organisms experience low pH during reproductive conditioning, environmental cues may be integrated in the germline through DNA methylation and other epigenetic modifications (Bell and Hellmann, 2019). Sex-associated methylation differences have been documented in C. gigas, and OA exposure modified the reproductive tissue methylome in C. gigas and C. virginica (Venkataraman et al, 2020;Sun et al, 2022;Venkataraman et al, 2022). Changes to DNA methylation due to low pH may impact successful reproduction or explain intergenerational effects of these conditions on marine invertebrates.…”

Latitudinal variation and plasticity in response to temperature in Geukensia demissa

“…When examining partial pressures of CO 2 , it was found that exposure to elevated levels caused proteins associated with the cytoskeleton, such as actin isoforms, and oxidative stress to be upregulated (Tomanek et al, 2011). Analysis of gonad methylomes in Pacific oysters also showed genes associated with protein ubiquitination to be differentially methylated in response to differing pH levels (Venkataraman et al, 2022). Here, we found that glutathione S-transferase was upregulated in GA and MA at 20°C, and higher activity of this protein has been found in M. edulis extracted from sites with high pollution (Fitzpatrick et al, 1997), which can alter pH levels.…”