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

Abstract

Alternative splicing is a fundamental mechanism of gene expression regulation that increases mRNA diversity and can be partially regulated by the circadian clock. 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 determined the impact of future ocean acidification conditions on circadian splicing patterns in the brain of fish, while accounting for diel CO2 fluctuations that naturally occur on coral reefs. The temporal splicing pattern observed across a 24-hour period in fish from the control group was largely absent in those exposed to either stable or fluctuating elevated CO2 conditions. Splicing patterns were influenced not only by an overall increase in CO2 concentration but also by its stability, with 6am and 6pm emerging as key timepoints when the majority of aberrant splicing events were identified. We found that fish in fluctuating CO2 conditions exhibited increased temporal plasticity in splicing events compared to fish in stable CO2 conditions. This was especially notable for genes associated with neural functioning. Our findings suggest that natural temporal splicing patterns in fish brains are disrupted by elevated CO2 exposure, with CO2 stability also influencing molecular responses. The increased plasticity in temporal splicing activity observed in fish in fluctuating CO2 environments may provide greater flexibility in biological responses to external pH changes, potentially enabling them to better cope with future ocean acidification conditions.