Thriving in Oxygen While Preventing ROS Overproduction: No Two Systems Are Created Equal

Abstract

From 2.5 to 2.0 billion years ago, atmospheric oxygen concentration [O2] rose thousands of times, leading to the first mass extinction. Reactive Oxygen Species (ROS) produced by the non-catalyzed partial reduction of O2 were highly toxic eliminating many species. Survivors developed different strategies to cope with ROS toxicity. At the same time, using O2 as the final acceptor in respiratory chains increased ATP production manifold. Thus, both O2 and ROS were strong drivers of evolution, as species optimized aerobic metabolism while developing ROS-neutralizing mechanisms. The first line of defense is preventing ROS overproduction and two mechanisms were developed in parallel: 1) Physiological uncoupling systems (PUS), which increase the rate of electron fluxes in respiratory systems. 2) Avoidance of excess [O2]. However, it seems that as avoidance efficiency improved, PUSs became less efficient. PUS includes branched respiratory chains and proton sinks, which may be proton specific, the mitochondrial uncoupling proteins (UCPs) or unspecific, the mitochondrial permeability transition pore (PTP). High [O2] avoidance also involved different strategies: 1) Cell association, as in biofilms or in multi-cellularity allowed gas-permeable organisms (oxyconformers) from bacterial to arthropods to exclude O2. 2) Motility, to migrate from hypoxic niches. 3) Oxyregulator organisms: as early as in fish, and O2-impermeable epithelium excluded all gases and only exact amounts entered through specialized respiratory systems. Here we follow the parallel evolution of PUS and O2-avoidance, PUS became less critical and lost efficiency. In regard, to proton sinks, there is fewer evidence on their evolution, although UCPs have indeed drifted in function while in some species it is not clear whether PTPs exist.

The Effects of Lipoic Acid on Yolk Nutrient Utilization, Energy Metabolism, and Redox Balance over Time in Artemia sp.

“…In this study, the authors reported that when KCN was added first, it partially inhibited mitochondrial oxygen consumption (in our case, mitochondrial reductive capacity, Figure 2b), and was completely inhibited after adding octyl-gallate. As mentioned previously [41,42], oxyconformers present branched mitochondrial respiratory electron chains. Together with the well-known mitochondrial oxidative phosphorylation (OxPhos) components, other redox enzymes are present as alternative oxidases (AOX), which, as mentioned above, are inhibited by other molecules such as octyl-gallate [35].…”

Controlled oxygen delivery to power tissue regeneration

“…However, straightforward augmentation of oxygen supply in the constructs will not yield a sustainable general solution because high concentrations of oxygen (hyperoxia) can inadvertently lead to ROS overproduction 34 (Fig. 3 ).…”

How does mitochondria function contribute to aerobic performance enhancement in lizards?

“…Trained lizards exhibited lower resting metabolic rates and lower maximal mitochondrial respiratory capacity than controls, indicating differing whole-organism and mitochondrial adaptations in response to higher energy demands from exercise training. Individual mitochondria can respond to demands by adjusting activity within the electron transport chain such as proton concentrations contributing to proton-motive force across the inner mitochondrial membrane, which affects ATP synthesis, proton leak, and ROS production (Treberg et al, 2018;Koch et al, 2021;Mendez-Romero et al, 2022). When oxygen consumption is uncoupled from ATP synthesis, individual mitochondria found within different organisms can have similar OCR with very different ATP synthesis rates (Koch et al, 2021).…”