PCB-153 and temperature cause restructuring of goldfish membranes: Homeoviscous response to a chemical fluidiser

Abstract

Ortho-substituted PCBs intercalate between membrane phospholipids similarly to cholesterol and increase fluidity. Ectothermic animals have a well-developed homeoviscous response to counter the fluidising effect of temperature and avoid the disruption of membrane proteins. However, it remains unknown whether chemical fluidisation can also activate a homeoviscous response or interfere with normal acclimation to temperature. The fatty acid composition and cholesterol content of membranes from gill, white muscle, liver, and brain was measured in goldfish exposed to 4 treatments in a 2×2 factorial design (acclimated to 5 or 20°C, and exposed or not to PCB-153). The expression of Δ6 and Δ9 desaturases was also measured in gill and liver because these enzymes modulate changes in membrane unsaturation. We hypothesised that thermal and chemical stress would cause similar adjustments in phospholipid unsaturation, membrane cholesterol, and desaturase expression. Results show that PCB-153 triggers a homeoviscous response by changing cholesterol content in liver (+51%) and brain (+216%), as well as the double bond index in gills (−17%). In response to higher temperature, the membranes of gill, muscle, and brain substitute polyunsaturated fatty acids such as arachidonate [20:4] and eicosadienoate [20:2] with saturated fatty acids such as palmitate [16:0] and stearate [18:0]. Each tissue has a distinct pattern of changes, suggesting that different local factors contribute to the stress response. It is also possible that the thermal tolerance of individual species influences the homeoviscous response because the changes observed in goldfish liver are not consistent with what has been reported for trout liver. No evidence supporting the activation of desaturase expression could be found. Overall, and contrary to expectation, modulating membrane cholesterol is the main mechanism used to cope with PCB-153, whereas changes in unsaturation dominate temperature acclimation. If also present in other species, these protective responses may prove particularly important for polar fish that face the combined effects of thermal stress from climate change and chemical stress from organochlorine deposition. This study is the first to show that in vivo exposure to a membrane fluidiser can cause a homeoviscous response in an ectothermic animal. We conclude that the homeostatic mechanisms that preserve normal membrane function vary: (1) with the nature of the stress that perturbs fluidity, (2) with local conditions within each tissue, and (3) possibly with the thermal tolerance of individual species. These complicating factors will have to be considered in future studies of homeoviscous adjustments.