Environmental conditioning of clams to low pH enhances robustness to environmental stress through acclimatory gene expression

Sub-lethal exposure to environmental stress may enhance ability to cope with repeated or novel environmental change, a process known as stress priming. In a previous study, post-larval acclimation to hypercapnic seawater improved growth and oxidative status of juvenile Pacific geoduck Panopea generosa (Gurr et al. 2021), indicating the potential for transcriptional shifts to drive modified organismal and cellular phenotypes. Juvenile clams were sampled and TagSeq gene expression data analyzed after acclimated at the pediveliger stage under ambient (921 µatm) and moderately-elevated pCO2 (2870 µatm) for 110 days (40-150 days post-fertilization; day 0) and subsequently after exposure in a reciprocal fashion to a second 7-day exposure (day 7), a 7-day return to ambient pCO2 (day 14), and a third 7-day exposure (day 21). Following acclimation, there were three and two pCO2 treatments under the second (ambient: 754 µatm; moderately-elevated: 2750 µatm; severely-elevated: 4940 µatm) and third exposures (ambient: 967 µatm; moderately-elevated: 3030 µatm). Across timepoints, stress-primed geoducks expressed sets of genes that had higher expression relative to naïve animals. Genes in processes identified with GO and pathway enrichment included histone methyltransferases and transcription factors, illustrating that moderate-stress history may frontload transcriptional regulation modifiers. Further, stress-primed clams were responsive to subsequent encounters, as functional analysis included quality control of mitochondria and immune defense under hypercapnic seawater and energy metabolism and biosynthesis under ambient recovery. In contrast, naïve clams expressed larger sets of genes with higher expression and were enriched for fatty-acid degradation and glutathione components at all timepoints, suggesting depletion of endogenous fuels and unsustainable energetic requirements if changes in carbonate chemistry exacerbated or persisted. Collectively, our transcriptomic data suggests post-larval acclimatory periods to low pH can, via gene expression regulation, enhance robustness to environmental stress in juvenile P. generosa. Such stress priming approaches may be beneficial for aquaculture husbandry practices, as global seafood demand intensifies concurrent with increasing climate change in marine systems.