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Oxidative metabolism meets the majority of vertebrate energy demands through the coupling of mitochondrial respiration to ATP production (OXPHOS). In endotherms, variations in OXPHOS coupling efficiency influence metabolic thermogenesis, locomotor economy and reactive oxygen species (ROS) generation. However, the extent of these variations and their functional implications in ectotherms are less clear. We measured mitochondrial oxygen consumption, ATP production and ROS production in permeabilized skeletal muscle fibres from salamanders, frogs and lizards representing ectotherm clades with low, medium and high standard metabolic rates (SMRs), respectively. Consistent with predicted associations with SMR, lizards had the highest capacities for muscle mitochondrial ATP production, while salamanders had the lowest. Unexpectedly, corresponding rates of oxygen consumption followed an opposite trend, reflecting 8.5-fold variations in OXPHOS coupling efficiency between salamanders (the lowest) and lizards (the highest). Intrinsic proton permeability of the inner mitochondrial membrane was the primary source of OXPHOS coupling variation across species, being highest in salamanders and lowest in lizards. Basal proton leak mediated by uncoupling proteins and the adenine nucleotide translocase was only seen in lizards, where it limits mitochondrial ROS production. We infer that diverse evolutionary selection pressures drive unexpectedly wide variations in muscle OXPHOS efficiency with different functional implications across ectotherm clades.
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Hypothesized Evolutionary Consequences of the Alternative Oxidase (AOX) in Animal Mitochondria
Abstract The environment in which eukaryotes first evolved was drastically different from what they experience today, and one of the key limiting factors was the availability of oxygen for mitochondrial respiration. During the transition to a fully oxygenated Earth, other compounds such as sulfide posed a considerable constraint on using mitochondrial aerobic respiration for energy production. The ancestors of animals, and those that first evolved from the simpler eukaryotes have mitochondrial respiratory components that are absent from later-evolving animals. Specifically, mitochondria of most basal metazoans have a sulfide-resistant alternative oxidase (AOX), which provides a secondary oxidative pathway to the classical cytochrome pathway. In this essay, I argue that because of its resistance to sulfide, AOX respiration was critical to the evolution of animals by enabling oxidative metabolism under otherwise inhibitory conditions. I hypothesize that AOX allowed for metabolic flexibility during the stochastic oxygen environment of early Earth which shaped the evolution of basal metazoans. I briefly describe the known functions of AOX, with a particular focus on the decreased production of reactive oxygen species (ROS) during stress conditions. Then, I propose three evolutionary consequences of AOX-mediated protection from ROS observed in basal metazoans: 1) adaptation to stressful environments, 2) the persistence of facultative sexual reproduction, and 3) decreased mitochondrial DNA mutation rates. Recognizing the diversity of mitochondrial respiratory systems present in animals may help resolve the mechanisms involved in major evolutionary processes such as adaptation and speciation.
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- Award ID(s):
- 1754152
- PAR ID:
- 10154598
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 4
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 994 to 1004
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icz015
