Hydrogen sulfide, reactive sulfur species and coping with reactive oxygen species

Life began in a ferruginous (anoxic and Fe2+ dominated) world around 3.8 billion years ago (bya). Hydrogen sulfide (H2S) and other sulfur molecules from hydrothermal vents and other fissures provided many key necessities for life's origin including catalytic platforms (primordial enzymes) that also served as primitive boundaries (cell walls), substrates for organic synthesis and a continuous source of energy in the form of reducing equivalents. Anoxigenic photosynthesis oxidizing H2S followed within a few hundred million years and laid the metabolic groundwork for oxidative photosynthesis some half-billion years later that slightly and episodically increased atmospheric oxygen around 2.3 bya. This oxidized terrestrial sulfur to sulfate which was washed to the sea where it was reduced creating vast euxinic (anoxic and sulfidic) areas. It was in this environment that eukaryotic cells appeared around 1.5 bya and where they evolved for nearly 1 billion additional years. Oxidative photosynthesis finally oxidized the oceans and around 0.6 bya oxygen levels in the atmosphere and oceans began to rise toward present day levels. This is purported to have been a life-threatening event due to the prevalence of reactive oxygen species (ROS) and thus necessitated the elaboration of chemical and enzymatic antioxidant mechanisms. However, these antioxidants initially appeared around the time of anoxigenic photosynthesis suggesting a commitment to metabolism of reactive sulfur species (RSS). This review examines these events and suggests that many of the biological attributes assigned to ROS may, in fact, be due to RSS. This is underscored by observations that ROS and RSS are chemically similar, often indistinguishable by analytical methods and the fact that the bulk of biochemical and physiological experiments are performed in unphysiologically oxic environments where ROS are artifactually favored over RSS.