Ocean Warming and Heat Stress Impact Molecules of Keystone Significance in a Predatory Marine Gastropod

Abstract

Water temperature is a major abiotic driver, controlling the rates and nature of biochemical reactions and subsequently affecting the physiology of marine organisms. However, relatively little is known about the implications of heat stress or predicted ocean climate change on marine secondary metabolites. The predatory gastropod Dicathais orbita is a useful model organism for climate change and natural product studies. Here we determine the upper thermal limit (CTMax) of D. orbita and investigate the effects of thermal stress on the bioactive compounds stored in their biosynthetic organ, the hypobranchial gland. Two CTMax experiments were undertaken, along with a static heat stress experiment where whelks were exposed to an elevated temperature of 30°C for one week, compared to a 20°C seawater control. An additional 35-day ocean climate change experiment used combinations of temperature (ambient: 23°C and future: 25°C) and pCO2 (ambient: ~380 ppm and future: ~765 ppm). The impacts on secondary metabolites in all experiments were assessed using liquid chromatography-mass spectrometry. The mean CTMax of the whelks, from the northern limit of their distribution, was found to be 35.2°C using a rapid temperature increase rate of 1°C/1 h, but was only 30.6°C when a gradual heating rate of 1°C/12 h was used. The overall composition of the secondary metabolites was significantly affected by heat stress in all four experiments, but not by elevated pCO2 in the ocean climate change experiment. The proportion of the choline ester murexine was significantly reduced in heat-stressed snails compared to the controls. Tyrindoxyl sulphate was significantly reduced under prolonged exposure to future temperature, whereas the relative abundance of the oxidation product, 6-bromoisatin significantly increased with elevated temperature exposure. Despite the fact that intertidal gastropods like D. orbita might be able to buffer the impact of external temperatures within the predicted future range, this study provides evidence that ocean warming could have significant implications for secondary metabolite production and/or storage in marine invertebrates. Impacts on bioactive molecules with multifunctional ecological roles could have implications for predator populations with possible flow on effects in some marine communities.