Transcriptomic profiling of adaptive responses to ocean acidification

Abstract

Some populations of marine organisms appear to have inherent tolerance or the capacity for acclimation to stressful environmental conditions, including those associated with climate change. Sydney rock oysters from the B2 breeding line exhibit resilience to ocean acidification (OA) at the physiological level. To understand the molecular basis of this physiological resilience, we analysed the gill transcriptome of B2 oysters that had been exposed to near-future projected ocean pH over two consecutive generations. Our results suggest that the distinctive performance of B2 oysters in the face of OA is mediated by the selective expression of genes involved in multiple cellular processes. Subsequent high-throughput qPCR revealed that some of these transcriptional changes are exclusive to B2 oysters and so may be associated with their resilience to OA. The intracellular processes mediated by the differentially abundant genes primarily involve control of the cell cycle and maintenance of cellular homeostasis. These changes may enable B2 oysters to prevent apoptosis resulting from oxidative damage or to alleviate the effects of apoptosis through regulation of the cell cycle. Comparative analysis of the OA conditioning effects across sequential generations supported the contention that B2 and wild-type oysters have different trajectories of changing gene expression and responding to OA. Our findings reveal the broad set of molecular processes underlying transgenerational conditioning and potential resilience to OA in a marine calcifier. Identifying the mechanisms of stress resilience can uncover the intracellular basis for these organisms to survive and thrive in a rapidly changing ocean.

The capacity of oysters to regulate energy metabolism‐related processes may be key to their resilience against ocean acidification

“…() recently showed that the greater responsiveness of selectively bred Sydney rock oysters to OA is due to their better capacity to compensate for CO 2 ‐induced extracellular acid‐base disturbances, by eliminating metabolic CO 2 through higher and more energy efficient filtration rates. Differential responses to CO 2 stress between populations of Sydney rock oysters have also been previously investigated at the protein and transcriptional levels (Goncalves et al., , ; Thompson et al., ). Proteomic analysis revealed that the majority of the differentially regulated proteins were found at lower concentrations in the gills of selectively bred oysters under CO 2 stress relative to ambient conditions, suggesting potential cellular injury.…”

“…In contrast, wild type oysters exhibited an up‐regulation of their differential proteins in response to elevated CO 2 (Thompson et al., ). At the level of gene expression, transgenerational exposure to elevated CO 2 (three consecutive generations) resulted in the differential regulation of genes associated with antioxidant defence, metabolism and the cytoskeleton in selectively bred oysters, while less pronounced changes in transcript levels were observed in wild type oysters (Goncalves et al., , ).…”

“…In contrast, wild type oysters exhibited an up-regulation of their differential proteins in response to elevated CO 2 . At the level of gene expression, transgenerational exposure to elevated CO 2 (three consecutive generations) resulted in the differential regulation of genes associated with antioxidant defence, metabolism and the cytoskeleton in selectively bred oysters, while less pronounced changes in transcript levels were observed in wild type oysters (Goncalves et al, 2016(Goncalves et al, , 2017 2015). However, Parker et al (2012) have shown that the SMR of selectively bred Sydney rock oysters increases following a 5-week exposure to elevated CO 2 (856 latm pCO 2 , pH 7.9), while no major increase is observed in wild type oysters.…”

Ocean acidification promotes broad transcriptomic responses in marine metazoans: a literature survey

“…The Sydney rock oyster, Saccostrea glomerata, has experienced decades of artificial selection for growth and disease resistance, which interestingly also corresponds to resilience against low pH [105,128,129]. This resilient family of oysters shows increases in resting metabolic rates [105] and in genes associated with the CSR and immune system, such as HSPs, antioxidant enzymes glutathione Stransferases and C1q domain proteins under ambient conditions [55,56]. These enzymes are then downregulated under transgenerational moderate pCO 2 (625 μatm) when compared to a control family [55,56].…”

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

“…Transcriptomic studies have proven to be a powerful approach for identifying genes and understanding pathways that shape organismal response to OA, and have been used to help elucidate potential trade-offs that result from acclimatization (Evans and Hofmann, 2012) , including genes associated with biomineralization, acid-base regulation, and metabolic function (Evans et al, 2013;Davies et al, 2016;Li et al, 2016;Goncalves et al, 2017;Wong et al, 2018;Griffiths et al, 2019) . From this literature it has been hypothesized that there is a trade-off between maintaining calcification versus other core functions (Wood et al, 2008) , whereby increased or sustained calcification under continued exposure may become too costly over time.…”