Hugo Kano

By Roberto C. Burini, Hugo T. Kano and Yong-Ming Yu

Organismal evolution led to innovations in metabolic pathways, many of which certainly modified the surface chemistry of the Earth. Volcanic activity introduced inorganic compounds (H2, CO2, CH4, SO2, and H2S) driving the metabolism of early organisms of the domains archaea and bacteria. In the absence of light, H2S and Fe2+ would have been the major electron donors and the electron acceptors could be either oxidized species such as the sulfurs, sulfate, and elemental sulfur, or carbon dioxide by the fermentation of acetate (forming methane). Elemental sulfur was produced by the reaction between H2S and SO2, while anoxygenic photosynthesis may have provided the sulfate which removed oceanic ferrous iron by its precipitation as sulfide into sediments. Hence, the sulfur cycle participation in life evolution comes from ancient anoxygenic elemental sulfur reduction generating environmental sulfide incorporated as mitochondrial Fe-S for the electron-transport chains. Anoxygenic photosynthesis may have provided the necessary sulfate to promote the evolution of sulfate-reducing bacteria. The evolution of oxygenic photosynthesis provided for diverse metabolic possibilities including non-photosynthetic sulfide oxidation, nitrification, and methanotrophy. An increase in oxygen levels would account for oxidative sulfur cycle, evolution of colorless sulfur bacteria, and emergence of large multicellular animals. Oxygen, initially a waste product of photosynthesis, first reacted with sulfur, iron or methane and latter accumulated in atmosphere resulting in more carbon production. Oxygenic photosynthesis becomes a positive feedback on the oxidation of the Earth-surface environment causing the growth and stabilization of continental platforms and carbon burial with more atmosphere oxidation. An increase in oxygen levels would account for oxidative sulfur cycle, evolution of colorless sulfur bacteria, and emergence of large multicellular animals. Oxygen enabled more efficient energy transformation from dietary food to ATP. However, evolution for mammals living on dry land has been closely linked to the adaptation of changes in O2 concentration in the environment, which means mitochondrial aerobic respiration. By using ancestral geochemistry of iron-sulfur clusters at the protein complexes I and II, the respiratory chains become badly insulated wires in the presence of oxygen (with reduced respiratory complexes) and there is leakage of electrons on to molecular oxygen. The electron leakage results in the formation of superoxide anion (SO) that remains within the mitochondrial matrix. If not promptly detoxified by anti-oxidative defenses, SO and its derived-oxidative species can alter cell signaling or attack cell structures leading to cell apoptosis. Sulfur-containing compounds participate either in oxidative stress generation (at endoplasmatic reticulum) or in (thiol) antioxidant defenses (mainly glutathione), thus functioning as redox sensing for enzyme activity and gene expression. Sulfur compounds that contributed for electron leakage and oxidative stress have counteractions by thiol participation either as antioxidant defensors and/or as redox-modulators or cell functions, influencing life evolution and contemporary diseases.

Part of the book: Glutathione in Health and Disease