Ocean acidification induces changes in circadian alternative splicing profiles in a coral reef fish

Abstract

Background Alternative splicing is a fundamental mechanism of gene expression regulation that increases the mRNA diversity expressed from the genome and can be partially regulated by the circadian clock. The time-dependent production of transcript isoforms from the same gene facilitates coordination of biological processes with the time of day and is a crucial mechanism enabling organisms to cope with environmental changes. In this study, we aim to determine the impact of future ocean acidification conditions on circadian splicing patterns in the brain of fish, while also accounting for diel CO₂ fluctuations that naturally occur on coral reefs. Results Fish in the control group exhibited a temporal splicing pattern across the 24-hour period, however, these splicing events were largely absent in fish exposed to either stable or fluctuating elevated CO₂ conditions. Furthermore, the molecular responses were influenced not only by an overall increase in CO₂ concentration but also by its stability, with 6am and 6pm being key timepoints when the majority of the aberrant splicing events were identified. We found that fish in fluctuating CO₂ conditions exhibited increased plasticity in transcriptional regulation by varying the proportion of transcript isoforms depending on the time-of-day. This was especially notable for genes associated with neural functioning. Conclusions Our findings suggest that fish rely on different molecular mechanisms to respond to elevated CO₂ exposure in stable and fluctuating conditions. Periodic variation in CO₂ levels in the fluctuating CO₂ treatment might enable fish to rely on feed-forward mechanisms to synchronize neural functions with external environmental conditions. Such interconnectedness between external pH changes and transcriptional regulation via alternative splicing may provide fish in fluctuating CO₂ environments with greater flexibility in biological responses, which may alleviate sensory and behavioural impairments enabling them to better cope with future ocean acidification conditions.