The Role of Hydrogen Sulfide in Evolution and the Evolution of Hydrogen Sulfide in Metabolism and Signaling

Abstract

The chemical versatility of sulfur and its abundance in the prebiotic Earth as reduced sulfide (H2S) implicate this molecule in the origin of life 3.8 billion years ago and also as a major source of energy in the first seven-eighths of evolution. The tremendous increase in ambient oxygen ∼ 600 million years ago brought an end to H2S as an energy source, and H2S-dependent animals either became extinct, retreated to isolated sulfide niches, or adapted. The first 3 billion years of molecular tinkering were not lost, however, and much of this biochemical armamentarium easily adapted to an oxic environment where it contributes to metabolism and signaling even in humans. This review examines the role of H2S in evolution and the evolution of H2S metabolism and signaling.

Catalase as a sulfide-sulfur oxido-reductase: An ancient (and modern?) regulator of reactive sulfur species (RSS)

“…The toxicity of H 2 S and other sulfur compounds are well known [39] and sulfur toxicity may have been an even greater problem early in evolution when these sulfur molecules were more prevalent [1]. In fact, the ability of catalase to metabolize H 2 S and polysulfides may have taken its origin in these sulfidic environments.…”

“…Although still somewhat controversial, a strong case can be made that H 2 S emanating from hydrothermal vents provided this energy as well as creating the chemical backbone for the earliest catalysts and cell walls [1]. Escape from the chemotrophic existence probably came within the next few hundred million years (~3.6 bya) in the form of anoxigenic photosynthesis [78], [79].…”

“…Reactive sulfide species (RSS) are chemically, biochemically and physiologically similar to ROS [1] and can be produced from sequential one-electron oxidations of hydrogen sulfide (H 2 S) to form a thiyl radical (HS • ), hydrogen persulfide (H 2 S 2 ) and persulfide radical (HS 2 •- ) before terminating in elemental sulfur (S 2 ); the latter usually cyclizing to S 8 ;.H 2 S (+e - ) --> HS • (+e - ) --> H 2 S 2 (+e - ) --> HS 2 •- (+e - ) --> S 2 …”

“…However, because catalase appears to have appeared in evolution long before oxygen was present and at a time when RSS were more likely to be involved in cellular metabolism [1], (also see discussion), we wondered if catalase could also dismutate persulfide, i.e. ;2H 2 S 2 –> 2H 2 S + S 2 …”

Garlic oil polysulfides: H2S- and O2-independent prooxidants in buffer and antioxidants in cells

“…Both prooxidant and antioxidant activities have been ascribed to H 2 S and related polysulfides (H 2 S n ; n ϭ 2-8), although there is increasing evidence that their prooxidant effects are considerably more prevalent than originally thought (8,40). Arguably, the greatest interest in H 2 S and polysulfide signaling is in their ability to bind to a protein cysteine through a process called sulfhydration, or more appropriately persulfidation (11), and, thereby, change the functional properties of that protein (11,19,20,37,44).…”