Brain transcriptome of gobies inhabiting natural CO2 seeps reveal acclimation strategies to long-term acidification

Abstract

Changes in ocean chemistry resulting from increasing acidification have direct impacts on the physiology and behaviour of teleosts. Ocean acidification (OA) can also affect species behaviour, survival and fitness with repercussions at population, community and ecosystem levels. Volcanic CO2 seeps offer a unique opportunity to study in situ both the direct and indirect effects of OA on fish and investigate their potential for acclimation. Here, we used the natural CO2 seeps in Vulcano Island, Italy to study the effects of OA on the brain transcriptome of the anemone goby, a species with high population density in the CO2 seeps. When compared to fish from environments with ambient pCO2, gobies living in acidified waters showed differences in expression of transcripts involved in ion transport and pH homeostasis, cellular stress, and immune response indicating their capability to mitigate CO2 induced oxidative stress and maintain physiological pH. We also found evidence of potential adaptive mechanisms to restore the functioning of GABA, whose activity can be affected by exposure to elevated CO2 levels. There was also a conspicuous difference in expression of core circadian rhythm transcripts which could provide an adaptive advantage by increasing flexibility of physiological processes under acidified conditions. Additionally, an overall increase in metabolism in fish from the CO2 seep indicates the ability to meet increased energetic costs associated with living in an acidified environment. Our results show potential molecular processes of acclimation to elevated pCO2 in gobies enabling them to thrive in the acidified waters of Vulcano Island.

Cross-talk between tissues is critical for intergenerational acclimation to environmental change

“…Notably, potassium channels, known for their significance in pH regulation and association with CO 2 chemoreception in the gills (Qin et al, 2010), displayed differential expression in the developmental treatment, possibly triggered by hypercapnia. This, in turn, could prompt downstream compensatory responses to maintain pH homeostasis (Suresh et al, 2023, Qin et al, 2010). However, the restoration of expression levels of these genes to control levels in intergenerationally treated fish suggests that intergenerational exposure may enhance and facilitate improved pH regulatory mechanisms.…”

Neuromolecular responses in disrupted mutualistic cleaning interactions under future environmental conditions

“…This response may also be related to changes in the circadian rhythm found altered for L. dimidiatus. High CO 2 commonly alters the transcriptional regulation of the circadian pathway in fish brains across many species, including coral reef fishes (Kang et al, 2022;Schunter et al, 2016Schunter et al, , 2021Suresh et al, 2023). Although further studies are needed to corroborate the link and its mechanism under ocean acidification, pH changes have the potential to alter the visual perception of cleaners, including the speed of processing images, which is a crucial ability to recognize clients as well as consolidate long-standing cleaning relationships (Tebbich et al, 2002).…”