Biological oxidation: over a century of hardship for the concept of active oxygen

Abstract

After much research in the field of biological oxidation, two main concepts of the mechanism of energy gain were consecutively proposed--the concept of direct oxygen activation (analogous to combustion), and the concept of activation of hydrogen followed by gradual energy release (analogous to putrefaction). The latter concept currently dominates. According to it, practically all the energy required in life is gained initially in the form of ATP; the latter being synthesized mostly due to the classical oxidative phosphorylation process. Direct activation of oxygen is considered to be a secondary pathway in its utilization, unrelated to bioenergetics. Besides, this pathway seems to be risky, since reactive oxygen species (ROS) are produced on account of it. However, evidence has been accumulated that a considerable part of all oxygen consumption undergoes direct activation; and this share increases with energy demand. Recent data also argues that ROS are indispensable for regulating biological function at all levels of biological organization. In spite of intense activation of oxygen, the usual levels of ROS in cells and tissues are extremely low due to their immediate elimination by the powerful an "antioxidant defense" system. In the process of elimination of ROS, high density energy (energy of electronic activation), equivalent to the energy of photons of visible and UV-light, is necessarily released, which has a much higher grade than the energy released in putrefaction. Both previous and more recent data argue that the energy of electronic excitation is biologically significant. The role of an aqueous environment with unusual water structuring in managing this form of energy in biology will also be discussed. Thus, the processes of oxygen activation in aqueous systems seem to be no less fundamental than the processes of activation of hydrogen atoms in organic fuels. Current bioenergetics has to consider both oxygen and hydrogen activation rather than concentrate on only one mode of energy gain and utilization.