Crucian carp (Carassius carassius) is one of the most anoxia-tolerant vertebrates. While physiological underpinnings of its ability to withstand O2 deprivation are well studied, the ability to tolerate the return to normoxia is still enigmatic. Such reoxygenation is associated with detrimental oxidation damage in other organisms, where mitochondria play a central role in the damaging effects. This leads to the question whether mitochondrial adaptations play a central role in the anoxia and reoxygenation tolerance of crucian carp. We here addressed whether mitochondria from crucian carp circumvent the negative effects of anoxia-reoxygenation exposure, namely the generation of reactive oxygen species (ROS) and subsequent oxidative stress. Crucian carp brain and heart mitochondria generated up to 4-fold less hydrogen peroxide (H2O2; a major ROS) compared to the closely related, anoxia-intolerant, common carp (Cyprinus carpio). The lower H2O2 emission was partly explained by higher (∼15-30%) total oxidant scavenging capacity. Complex II-mediated flux was ∼40% reduced after anoxia-reoxygenation in crucian carp heart mitochondria. Mitochondrial H2O2 generation measured in vivo was unaffected by anoxia-reoxygenation exposure in heart, brain and gill, but reduced by ∼25% in liver. There were also tissue-specific increases in protein carbonylation (∼1.8-fold in brain and gills) and mitochondrial DNA (mtDNA) damage (∼1.5-fold in liver and heart), indicating that biphasic oxidative stress responses affect tissues differently. Our data show that crucian carp avoids excessive mitochondrial ROS generation upon exposure to anoxia-reoxygenation. The tissue-specific distribution of protein and mtDNA oxidation indicate that crucian carp balances body redox signalling to secure resilience during fluctuating O2 availability.
Lau et al. (Fri,) studied this question.