Oxygen: From Toxic Waste to Optimal (Toxic) Fuel of Life

Abstract

Some . billion years ago, the great oxygenation event (GOE) led to a -fold rise in atmospheric oxygen [O ], killing most species on Earth. In spite of the tendency to produce toxic reactive oxygen species (ROS), the highly exergonic reduction of O made it the ideal biological electron acceptor. During aerobic metabolism, O is reduced to water liberating energy, which is coupled to adenosine triphosphate (ATP) synthesis. Today, all organisms either aerobic or not need to deal with O toxicity. O -permeant organisms need to seek adequate [O ], for example, aquatic crustaceans bury themselves in the sea botom where O is scarce. Also, the intestinal lumen and cytoplasm of eukaryotes is a microaerobic environment where many facultative bacteria or intracellular symbionts hide from oxygen. Organisms such as plants, ish, reptiles and mammals developed O -impermeable epithelia, plus specialized external respiratory systems in combination with O -binding proteins such as hemoglobin or leg-hemoglobin control [O ] in tissues. Inside the cell, ROS production is prevented by rapid O consumption during the oxidative phosphorylation (OxPhos) of ATP. When ATP is in excess, OxPhos becomes uncoupled in an efort to continue eliminating O . Branched respiratory chains, unspeciic pores and uncoupling proteins (UCPs) uncouple OxPhos. One last line of resistance against ROS is deactivation by enzymes such as super oxide dismutase and catalase. Aerobic organisms proit from the high energy released by the reduction of O , while at the same time they need to avoid the toxicity of ROS.

Wolbachia pipientis grows in Saccharomyces cerevisiae evoking early death of the host and deregulation of mitochondrial metabolism

“…Avoidance, i.e. hiding from oxygen, is a common behavior in oxyconformers (Rosas‐Lemus et al., ). In air, oxygen saturation concentration is ~21% (200 μmol L −1 ) while intracellular oxygen concentration ranges between 13.2% and 14% (126–133 μmol L −1 ) for rhabdomyosarcoma (RD) cells (Potter et al., ) or HEK293T cells (Abcam, ).…”

“…In our hands, Wolbachia infection resulted in activation of mitochondria beyond the stationary growth phase. It may be speculated that such activation constitutes an advantage for Wolbachia either due to quenching of oxygen in the cytoplasm (Rosas-Lemus et al, 2016) or because Wolbachia needs high ATP that an active mitochondria provides (Potter, Badder, Hoade, Johnston, & Morten, 2016). It has already been suggested by experiments using paraquat that Wolbachia sensitivity to free radicals is higher than that of the host (Fallon et al, 2013) and it cannot survive outside a host cell unless it is kept in a 5% CO 2 atmosphere (Rasgon et al, 2006).…”

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

“…Total avoidance of O 2 is observed in anaerobic organisms such as those living in animal digestive tubes ( Fenchel and Finlay, 1994 ). However, when accidentally exposed to high [O 2 ], anaerobic organisms may differentially express branched RCs ( Rosas-Lemus et al, 2016 ; Jayawardhane et al, 2020 ). Another avoidance strategy is association into biofilms, where surface cells limit O 2 diffusion, creating an anaerobic internal microenvironment ( Stewart, 2003 ).…”

“…The most sophisticated O 2 avoidance system first appeared in fish and evolved in amphibians, reptiles, birds, and mammals, which developed a gas-impermeable epithelium plus a specialized external respiratory system (gills or lungs) ( Stamati et al, 2011 ). These are the oxyregulator organisms where [O 2 ] reaching internal cells is 20–31 μM or four to five hundred times less that atmospheric [O 2 ] which is 1,026 μM at sea level ( Figure 1 ) ( Rosas-Lemus et al, 2016 ). Interestingly, amphibians already have lungs, even when their skin is still permeable to gases and participates in O 2 /CO 2 exchange (skin breathing) ( Tattersall, 2007 ).…”

“…Atmospheric [O 2 ] 1,028 μM, lung alveoli [O 2 ] 143 μM; capillaries [O 2 ] 130 mM; arteries [O 2 ] 123 μM; interstitial fluids [O 2 ] 55 μM; tissue cells [O 2 ] 31 μM; and mitochondria [O 2 ] 20 µM. Values from Rosas-Lemus et al, 2016 and references therein.…”