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

Abstract

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.

Ocean acidification induces subtle shifts in gene expression and DNA methylation in mantle tissue of the Eastern oyster (Crassostrea virginica)

“…In the present study, OA was associated with a genome-wide decrease in methylation (hypomethylation), similar to the response observed in pteropods (Bogan et al, 2020) , but opposite the response observed in corals (Putnam et al, 2016;Liew et al, 2018) . Over time, an increase in methylation (hypermethylation) was observed, also consistent with the DNA methylation response observed in pteropods (Bogan et al, 2020) . Unlike for the pteropods, the same degree of hypermethylation through time was observed in both the control and high OA treatments (i.e., no interaction between treatment and time).…”

“…This genome-wide DNA methylation response to OA has been found in several other species of marine calcifiers, including corals, pteropods, and in the gonadal tissue of C. virginica (Putnam et al, 2016;Liew et al, 2018;Bogan et al, 2020;Venkataraman et al, 2020) . In the present study, OA was associated with a genome-wide decrease in methylation (hypomethylation), similar to the response observed in pteropods (Bogan et al, 2020) , but opposite the response observed in corals (Putnam et al, 2016;Liew et al, 2018) . Over time, an increase in methylation (hypermethylation) was observed, also consistent with the DNA methylation response observed in pteropods (Bogan et al, 2020) .…”

“…At the transcriptomic level, this cost can manifest as shifts in the expression of both calcification and metabolic genes through time (Li et al, 2016) , suggesting that certain acclimatization responses may be unsustainable during extended exposure to OA. The precise mechanisms that mediate these changes in gene expression remain underexplored, but recent studies indicate that DNA methylation, an epigenetic modification, may be an important regulator of these responses Liew et al, 2018;Bogan et al, 2020) .…”

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

“…In addition, we also hypothesized that OA-induced shifts in the transcriptome of C. virginica would correspond to shifts in the methylome. This was based on growing evidence in the DNA methylation literature indicating that DNA methylation is linked with gene regulation (Zilberman et al, 2007;Zemach et al, 2010;Gavery and Roberts, 2013;Olson and Roberts, 2014;Dixon et al, 2018;Zhang et al, 2020), is induced by OA and other environmental stressors (Putnam et al, 2016;Dixon et al, 2018;Bogan et al, 2020), and corresponds with calcification response to OA in marine invertebrates (Liew et al, 2018).…”

“…At the transcriptomic level, this cost can manifest as shifts in the expression of both calcification and metabolic genes over time (Li et al, 2016), suggesting that certain acclimatization responses may be unsustainable during extended exposure to OA. The precise mechanisms that mediate these changes in gene expression remain underexplored, but recent studies indicate that DNA methylation, an epigenetic modification, may be an important regulator of these responses (Liew et al, 2018;Bogan et al, 2020).…”