Ocean acidification alters the transcriptomic response in the nervous system of Aplysia californica during reflex behaviour
Ocean acidification (OA) has numerous impacts on marine organisms, including impairments to crucial behaviours. While these behaviours are controlled in the brain or neuro system, it is the complexity of the nervous system that makes linking behavioural impairments to the environmental change difficult. Hence here we make use of a neurological model species with a well-studied simple neuro system and behaviours, the California sea hare (Aplysia californica). By exposing Aplysia to current day control (500 uatm) or predicted near-future CO2 conditions (1100 uatm), we test the effect of OA on their tail withdrawal reflex (TWR) and the underlying neuromolecular response of the pleural-pedal ganglia, the part of the nervous system known to be responsible for the TWR. We further investigate how OA affects learning processes and test whether altered GABA-mediated neurotransmission is involved in impaired TWR, as previously reported for other behavioural impairments. Under OA conditions, Aplysia relaxed their tails significantly faster and their nervous system expressed more mRNA precursor of sensorin-A, an inhibitor of the mechanosensory neurons. Impaired TWR was also accompanied by a large transcriptional reprogramming of genes involved in neurotransmission, vesicular transport, cellular signalling, as well as energetically expensive processes and stress. Habituation affected the molecular response to OA regarding vesicle transport and stress response functions and produced a sensitization-like behavioural response, showing that elevated CO2 can influence the neuronal and behavioural outputs associated with learning. Finally, exposure to a GABA antagonist, gabazine, did not restore normal behaviour and provoked little molecular response, indicating that acidification-induced TWR impairment occurs through other mechanisms than altered GABAergic neurotransmission for this reflex. Instead, cellular changes regarding neurotransmitter receptors and/or synaptic vesicle activity could be responsible for the observed reduction in prolonged tail contraction. Our study shows effects of ocean acidification on neurological systems that control for animal behaviour with further implications on learning experiences.