Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Abstract

Ocean acidification is the increase in seawater pCO 2 due to the uptake of atmospheric anthropogenic CO 2, with the largest changes predicted to occur in the Arctic seas. For some marine organisms, this change in pCO 2, and associated decrease in pH, represents a climate change‐related stressor. In this study, we investigated the gene expression patterns of nauplii of the Arctic copepod Calanus glacialis cultured at low pH levels. We have previously shown that organismal‐level performance (development, growth, respiration) of C. glacialis nauplii is unaffected by low pH. Here, we investigated the molecular‐level response to lowered pH in order to elucidate the physiological processes involved in this tolerance. Nauplii from wild‐caught C. glacialis were cultured at four pH levels (8.05, 7.9, 7.7, 7.5). At stage N6, mRNA was extracted and sequenced using RNA‐seq. The physiological functionality of the proteins identified was categorized using Gene Ontology and KEGG pathways. We found that the expression of 151 contigs varied significantly with pH on a continuous scale (93% downregulated with decreasing pH). Gene set enrichment analysis revealed that, of the processes downregulated, many were components of the universal cellular stress response, including DNA repair, redox regulation, protein folding, and proteolysis. Sodium:proton antiporters were among the processes significantly upregulated, indicating that these ion pumps were involved in maintaining cellular pH homeostasis. C. glacialis significantly alters its gene expression at low pH, although they maintain normal larval development. Understanding what confers tolerance to some species will support our ability to predict the effects of future ocean acidification on marine organisms.

Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

“…Notable were those related to the response and detection of stress, and actin organization and regulation. Actin regulation is linked to cytoskeleton maintenance and has been identified as responsive to low pH stress in copepods (39). In addition, we found strong allelic differences between lines in regulators of expression (Table S1), suggesting that trans-acting regulators may have been under selection and responsible for the adaptive changes in gene expression.…”

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

“…These studies emphasize that a core response of marine metazoans to decreases in pH involves a reallocation and/or changes in production of ATP, often as a trade-off in maintaining ion homeostasis, calcification and control of internal pH levels. Modulation of ATP-producing enzymes has also been reported in non-calcifying marine organisms in response to low pH, including Arctic copepods [66] and within brains of coral reef fish [89]. Another commonly reported gene expression signature that predicts metabolic depression is changes in genes involved in mitochondrial and oxidative metabolism.…”

“…Organisms employ different mechanisms of metabolic responses based on length of exposure to stressors. Upregulation of genes involved in lipid metabolism is observed in many studies of long-term pCO 2 stress response in a variety of taxa: reef-building corals [21,23,25,32], pteropods [62,63], and Arctic copepods [66]. Concurrently, there are studies reporting increased lipid content in corals after exposure to increased pCO 2 [111,112].…”

“…While studies have investigated metabolic rates and ATP production in response to pH [98], gene expression has become another tool to assess the potential for metabolic depression, especially to elucidate mechanisms of this response (Table 2). Gene expression studies reporting metabolic depression in marine metazoans include adult blue mussels [45], adult pearl oysters [50,51], purple sea urchin larvae [81,82], temperate brittle stars [72], clams [41], Arctic copepods [66], developing Medaka fish [93], marine polychaetes [37] and reef-building corals [21,[24][25][26]. Despite being commonly observed across gene expression studies in response to low pH, the means by which metabolic depression is characterized through gene expression data varies by study and taxon.…”

“…Studies of transcriptomic responses to high pCO 2 /low pH exposure in shell-forming zooplankton show dramatic modulation of energetic processes. Both Arctic copepods and Antarctic pteropods show massive downregulation of much of the transcriptome after low pH exposure (1700 μatm and 902 μatm, respectively) [62,66]. Decreased expression of mitochondrion and oxidative metabolism genes are also observed under high pCO 2 (720 μatm) in Mediterranean pteropods, including suppressed expression of the entire protein synthesis machinery [60].…”