Rapid evolution fuels transcriptional plasticity to ocean acidification

Abstract

Ocean acidification (OA) is postulated to affect the physiology, behavior, and life‐history of marine species, but potential for acclimation or adaptation to elevated pCO2 in wild populations remains largely untested. We measured brain transcriptomes of six coral reef fish species at a natural volcanic CO2 seep and an adjacent control reef in Papua New Guinea. We show that elevated pCO2 induced common molecular responses related to circadian rhythm and immune system but different magnitudes of molecular response across the six species. Notably, elevated transcriptional plasticity was associated with core circadian genes affecting the regulation of intracellular pH and neural activity in Acanthochromis polyacanthus. Gene expression patterns were reversible in this species as evidenced upon reduction of CO2 following a natural storm‐event. Compared with other species, Ac. polyacanthus has a more rapid evolutionary rate and more positively selected genes in key functions under the influence of elevated CO2, thus fueling increased transcriptional plasticity. Our study reveals the basis to variable gene expression changes across species, with some species possessing evolved molecular toolkits to cope with future OA.

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

“…One of them is synaptic transmission and the down regulation of a lincRNA and the neighbouring coding CACNA1E (gene voltage-gated calcium channel complex) can contribute to synaptic transmission (Berecki et al, 2014), which was also found to behave similarly to a previous RNAseq A. polyacanthus data (Schunter et al, 2018). In addition, immune responses are commonly associated with ocean acidification in fish including our study species (De Souza et al, 2014;Kang et al, 2022;Machado et al, 2020), and here we find differential expression of lincRNAs neighbouring a variety of immune response genes that show co-expression in a gene network significantly correlated with CO2 levels. This reveals that lincRNAs annotated in our coral reef fish show differential expression in response to an environmental factor, CO2 levels, and that some of these differentially expressed lincRNAs are in close proximity to coding genes that are known to have functional implications in the response to ocean acidification in fishes.…”

“…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.…”

“…To identify lncRNAs in the Acanthochromis polyacanthus genome, 226 RNA-seq samples were compiled from published studies investigating the effect of elevated CO2 on the brain transcriptome of A. polyacanthus (Kang et al, 2022;Schunter et al, 2018Schunter et al, , 2016PRJNA658203). This allows for a comprehensive annotation across the genome of lncRNAs associated with the exposure to elevated CO2 in laboratory and natural settings.…”

“…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.…”

Upwelling‐level acidification and pH/pCO2 variability moderate effects of ocean acidification on brain gene expression in the temperate surfperch, Embiotoca jacksoni

“…Many coastal ecosystems experience significant environmental variability over a range of temporal scales, including fluctuations in seawater pH/ p CO 2 (Chan et al, 2017; Hofmann et al, 2011; Kang et al, 2022; Kroeker et al, 2020). In upwelling regions, where deeper, more acidic water is brought to the ocean surface, pH can vary by half a unit over a period of weeks (Hirsh et al, 2020; Hofmann et al, 2011).…”