Are reactive oxygen species always bad? Lessons from hypoxic ectotherms

Abstract

ABSTRACT Oxygen (O2) is required for aerobic energy metabolism but can produce reactive oxygen species (ROS), which are a wide variety of oxidant molecules with a range of biological functions from causing cell damage (oxidative distress) to cell signalling (oxidative eustress). The balance between the rate and amount of ROS generated and the capacity for scavenging systems to remove them is affected by several biological and environmental factors, including oxygen availability. Ectotherms, and in particular hypoxia-tolerant ectotherms, are hypothesized to avoid oxidative damage caused by hypoxia, although it is unclear whether this translates to an increase in ecological fitness. In this Review, we highlight the differences between oxidative distress and eustress, the current mechanistic understanding of the two and how they may affect ectothermic physiology. We discuss the evidence of occurrence of oxidative damage with hypoxia in ectotherms, and that ectotherms may avoid oxidative damage through (1) high levels of antioxidant and scavenging systems and/or (2) low(ering) levels of ROS generation. We argue that the disagreements in the literature as to how hypoxia affects antioxidant enzyme activity and the variable metabolism of ectotherms makes the latter strategy more amenable to ectotherm physiology. Finally, we argue that observed changes in ROS production and oxidative status with hypoxia may be a signalling mechanism and an adaptive strategy for ectotherms encountering hypoxia.