The effect of acute warming on protein turnover and oxygen demand in stenothermal and eurythermal eelpouts

Abstract

The increase in CO2 in the atmosphere due to the burning of fossil fuels is the main cause of climate change and thus global warming. Climate change has fundamental consequences for all organisms, including marine life. Ectothermal organisms, such as fish, are particularly affected, since their body temperature is equal to their environment. Fish have adapted to diverse temperature conditions depending in different climatic regions and thus exhibit a range of temperature adaptations. Fish in polar regions, such as Antarctic fish species, are adapted to constantly cold temperatures, while fish in temperate regions are adapted to seasonal temperature fluctuations and can survive in wide temperature windows. Thermal adaptation can be investigated by acclimating fish to certain temperatures over a long period (long-term acclimation) or during acute temperature changes (acute warming). This study investigates the differences and similarities in thermal adaptions of stenothermal and eurythermal fish during acute warming events. For this comparison, the closely related eelpout species Pachycara brachycephalum from the Southern Ocean and Zoarces viviparus from the North Sea were selected as experimental animals. During these experiments, water temperature was increased from 0°C to 10°C at a rate of 2°C day-1 for P. brachycephalum. For Z. viviparus, the temperature was increased from 4°C to 22°C at a rate of 3°C day-1. Isotopically labelled phenylalanine was injected intraperitonially at several temperature levels (P. brachycephalum: 0, 2, 4, 6, 8 and 10°C; Z. viviparus: 4, 10, 13, 16, 22°C) and after 1.5- and 3-hours gill and white muscle tissues were sampled. Protein synthesis rate was determined in both tissue types and protein degradation analyzed in the muscle by measuring cathepsin D activity and via untargeted metabolic profiling using NMR (nuclear magnetic resonance). Furthermore, oxygen consumption was measured during acute warming to draw conclusions about energy requirements. In P. brachycephalum, the rate of protein synthesis in white muscle did not change with increasing temperature. In contrast, the protein synthesis rate in Z. viviparus increased up to 16°C and then decreased slightly at 22°C. Comparing the two species at a common temperature (4 and 10°C), the protein synthesis rate in P. brachycephalum was 2-3-times higher, while the activity of cathepsin D was 10 times higher in white muscle. Both the rate of protein synthesis in the gills and whole animal oxygen demand increased exponentially in both species and no differences were found between the species when compared at a common temperature. In conclusion, these data suggest that protein synthesis in P. brachycephalum is cold-compensated and is maintained at a high rate at low temperatures. The protein synthesis rate in the white muscle of Z. viviparus only reached that of P. brachycephalum near its thermal optimum. This cold adaptation may enable P. brachycephalum to survive in the world's coldest ocean. In contrast, Z. viviparus responds very quickly to temperature differences, which occur regularly in the North Sea.