Oxygen Stress and Superoxide Dismutases

THE OXYCEN PARADOX The accumulation of dioxygen in Earth's atmosphere al- lowed for the evolution of aerobic organisms that use O2 as the terminal electron acceptor, thus providing a higher yield of energy compared with fermentation and anaerobic respi- ration. For example, in aerobic metabolism, the complete breakdown of one molecule of glucose yields a total of 38 molecules of ATP, whereas the anaerobic breakdown of this same glucose molecule to ethanol and CO, yields only 8 ATPs. In its ground state, molecular O2 (dioxygen) is relatively unreactive, yet it is capable of giving rise to lethal reactive ,excited states as free radicals and derivatives. Utilization of O2 proceeds most readily via a complete stepwise, four- electron reduction to water during which partially reduced reactive intermediates are generated (Fig. 1). The reactive species of reduced dioxygen include the superoxide radical (. 02-), hydrogen peroxide (H202), and the hydroxyl radical (. OH). These and the physiologically energized form of dioxygen, singlet oxygen ('O2), are the biologically most important O2 species. An activation energy of approximately 22 kcal/mol is required to raise molecular O2 from its ground state to its first singlet state. In higher plants, this energy is readily obtained from light quanta via such transfer molecules as Chl (Foote, 1976). A11 of these activated oxygen species are extremely reactive and cytotoxic in a11 organisms. These highly reactive species can react with unsaturated fatty acids to cause peroxidation of essential membrane lipids in the plasmalemma or intracellular organelles. Peroxidation dam- age of the plasmalemma leads to leakage of cellular contents, rapid desiccation, and cell death. Intracellular membrane damage can affect respiratory activity in mitochondria, cause pigment breakdown, and cause loss of carbon-fixing ability in chloroplasts. Severa1 Calvin-cycle enzymes within chloroplasts are ex- tremely sensitive to H202, and high levels of H202 (the product of superoxide dismutation) directly inhibit C02 fix- ation (Kaiser, 1979). H202 has also been shown to be active with mixed function oxidases in marking severa1 types of enzymes for proteolytic degradation (Fucci et al., 1983). Su- peroxide and H202 can react in a "Haber-Weiss" reaction to generate the hydroxyl radical (+ OH), which is the most potent oxidant known. The hydroxyl radical indiscriminately and rapidly attacks virtually a11 macromolecules, leading to seri- ' Supported by the Environmental Biology Program of the U.S.