Diel CO₂ fluctuations alter the molecular response of coral reef fishes to ocean acidification conditions

Abstract

Environmental CO2 variation can modify the responses of marine organisms to ocean acidification, yet the underlying mechanisms for this effect remain unclear. On coral reefs, environmental CO2 fluctuates on a regular day-night cycle. Effects of future ocean acidification on coral reef fishes might therefore depend on their response to this diel cycle of CO2. To evaluate the effects on the brain molecular response, we exposed two common reef fishes (Acanthochromis polyacanthus and Amphiprion percula) to two projected future CO2 levels (750 and 1,000 microatmospheres) under both stable and diel fluctuating conditions. We found a common signature to stable elevated pCO2 for both species, which included the downregulation of immediate early genes, indicating lower brain activity. The transcriptional program was more strongly affected by higher average CO2 in a stable treatment than for fluctuating treatments, however, the largest difference in molecular response was between stable and fluctuating CO2 treatments. This indicates that a response to a change in environmental CO2 conditions is different for organisms living in a fluctuating than in stable environments. The differential regulation was related to steroid hormones and circadian rhythm (CR). Both species exhibited a marked difference in the expression of CR genes among CO2 treatments, possibly accommodating a more flexible adaptive approach to acid-base control, which could explain reduced impairment. Our results suggest that environmental CO2 fluctuations might enable reef fishes to phase shift their clocks and anticipate CO2 changes, thereby avoiding impairments and more successfully adjust to ocean acidification conditions.

Rapid evolution fuels transcriptional plasticity to ocean acidification

“…Elevated p CO 2 exposure has been shown to induce expression changes in the CR pathway in Ac . polyacanthus (Schunter et al, 2016) as well as an anemonefish, Amphiprion percula , in laboratory settings (Schunter et al, 2021). Three species in this study— D .…”

Environmental regulation of gene expression mediated by Long non-coding RNAs

“…Furthermore, lncRNAs have been shown to regulate core circadian rhythm genes in mammals (Mosig & Kojima, 2021). With a substantial fraction of lncRNAs affecting the gene expression of their neighbouring coding genes (Engreitz et al, 2016), it is no surprise to see elevated expression in lncRNAs neighbouring GABA A receptor and core circadian rhythm genes as these are known to play important roles in the transcriptional response to ocean acidification (Kang et al, 2022; Schunter et al, 2021, 2016). As our RNAseq data is from ocean acidification experiments, this now hints at a regulatory involvement of lncRNAs in these key functions.…”

“…For this, we use the spiny chromis Acanthochromis polyacanthus, a common coral reef fish in the Western Pacific, extensively studied for fish acclimation processes to environmental changes in the last decade. Generous RNA sequencing has been performed on this species (Bernal et al, 2022;Kang et al, 2022;Schunter et al, 2021Schunter et al, , 2016 to interpret its transcriptional responses to ocean environmental changes. This extensive knowledge on the transcriptional processes to ocean acidification in A. polyacanthus allows for a broad evaluation of the involvement of lncRNAs and provides a guideline for future studies also in other systems.…”

Neuro-molecular characterization of fish cleaning interactions

“…Of the final gene expression matrix we filtered out transcripts with no expression by using the script filter_low_expr_transcripts.pl while retaining the most highly expressed isoforms for each gene using the command -highest_iso_only. To statistically evaluate differential gene expression, we used DESeq2-package v. 1.26.0 [37] with a Wald test statistic with a design = ~treatment for each region of the brain separately, an FDR p-adjusted significance value of 0.05 and an absolute log2fold change threshold of 0.3 as a cut-off as previously used in other study evaluating fish brain transcriptomics [38] and to remove further potentially spurious significant differential expression. We compared the individuals from control vs interaction to determine their significant differential gene expression for the three regions of the brain forebrain (FB), midbrain (MB) and hindbrain (HB) to retrieve the molecular response specific to these areas for both species, but separately for each species.…”

“…Studies on this species as a model for behaviour, have focused on neural physiological responses in its interaction with other species and how different social situations such as the establishment of social bonds modulate their behaviour [14,[20][21][22]. For example, dopamine and serotonin levels influence the motivation of cleaners to engage in interactions [23] and are induced during social stress [38]. These monoaminergic hormones (dopamine and serotonin) also play a role in the regulation of the service of cleaning in this cleaner wrasse and their willingness to interact, thus modifying the capacity of individuals to react to new social scenarios (i.e.…”