Interspecific variation in brain mitochondrial complex I and II capacity and ROS emission in marine sculpins

Abstract

Environmental hypoxia presents a metabolic challenge for animals because it inhibits mitochondrial respiration and can lead to the generation of reactive oxygen species (ROS). We investigated the interplay between O 2 use for aerobic respiration and ROS generation among sculpin fishes (Cottidae, Actinopterygii) that are known to vary in whole-animal hypoxia tolerance. We hypothesized that mitochondria from hypoxia-tolerant sculpins would show more efficient O 2 use with a higher phosphorylation efficiency and lower ROS emission. We showed that brain mitochondria from more hypoxia-tolerant sculpins had lower complex I and higher complex II flux capacities compared with less hypoxia-tolerant sculpins, but these differences were not related to variation in phosphorylation efficiency (ADP/O) or mitochondrial coupling (respiratory control ratio). The hypoxia-tolerant sculpins had higher mitochondrial H 2 O 2 emission per O 2 consumed (H 2 O 2 /O 2 ) under oligomycin-induced state 4 conditions compared with less hypoxia-tolerant sculpins. An in vitro redox challenge experiment revealed species differences in how well mitochondria defend their glutathione redox status when challenged with high levels of reduced glutathione, but the redox challenge elicited the same H 2 O 2 /O 2 in all species. Furthermore, in vitro anoxia recovery lowered absolute H 2 O 2 emission (H 2 O 2 per mg mitochondrial protein) in all species and negatively impacted state 3 respiration rates in some species, but the responses were not related to hypoxia tolerance. Overall, we clearly demonstrate a relationship between hypoxia tolerance and complex I and II flux capacities in sculpins, but the differences in complex flux capacity do not appear to be directly related to variation in ROS metabolism.